diff --git a/changelog.d/13024.misc b/changelog.d/13024.misc
new file mode 100644
index 000000000..aa43c8242
--- /dev/null
+++ b/changelog.d/13024.misc
@@ -0,0 +1 @@
+Refactor methods in `synapse.api.auth.Auth` to use `Requester` objects everywhere instead of user IDs.
diff --git a/synapse/api/auth.py b/synapse/api/auth.py
index 523bad0c5..9a1aea083 100644
--- a/synapse/api/auth.py
+++ b/synapse/api/auth.py
@@ -37,8 +37,7 @@ from synapse.logging.opentracing import (
     start_active_span,
     trace,
 )
-from synapse.storage.databases.main.registration import TokenLookupResult
-from synapse.types import Requester, UserID, create_requester
+from synapse.types import Requester, create_requester
 
 if TYPE_CHECKING:
     from synapse.server import HomeServer
@@ -70,14 +69,14 @@ class Auth:
     async def check_user_in_room(
         self,
         room_id: str,
-        user_id: str,
+        requester: Requester,
         allow_departed_users: bool = False,
     ) -> Tuple[str, Optional[str]]:
         """Check if the user is in the room, or was at some point.
         Args:
             room_id: The room to check.
 
-            user_id: The user to check.
+            requester: The user making the request, according to the access token.
 
             current_state: Optional map of the current state of the room.
                 If provided then that map is used to check whether they are a
@@ -94,6 +93,7 @@ class Auth:
             membership event ID of the user.
         """
 
+        user_id = requester.user.to_string()
         (
             membership,
             member_event_id,
@@ -182,96 +182,69 @@ class Auth:
 
             access_token = self.get_access_token_from_request(request)
 
-            (
-                user_id,
-                device_id,
-                app_service,
-            ) = await self._get_appservice_user_id_and_device_id(request)
-            if user_id and app_service:
-                if ip_addr and self._track_appservice_user_ips:
-                    await self.store.insert_client_ip(
-                        user_id=user_id,
-                        access_token=access_token,
-                        ip=ip_addr,
-                        user_agent=user_agent,
-                        device_id="dummy-device"
-                        if device_id is None
-                        else device_id,  # stubbed
-                    )
-
-                requester = create_requester(
-                    user_id, app_service=app_service, device_id=device_id
+            # First check if it could be a request from an appservice
+            requester = await self._get_appservice_user(request)
+            if not requester:
+                # If not, it should be from a regular user
+                requester = await self.get_user_by_access_token(
+                    access_token, allow_expired=allow_expired
                 )
 
-                request.requester = user_id
-                return requester
+                # Deny the request if the user account has expired.
+                # This check is only done for regular users, not appservice ones.
+                if not allow_expired:
+                    if await self._account_validity_handler.is_user_expired(
+                        requester.user.to_string()
+                    ):
+                        # Raise the error if either an account validity module has determined
+                        # the account has expired, or the legacy account validity
+                        # implementation is enabled and determined the account has expired
+                        raise AuthError(
+                            403,
+                            "User account has expired",
+                            errcode=Codes.EXPIRED_ACCOUNT,
+                        )
 
-            user_info = await self.get_user_by_access_token(
-                access_token, allow_expired=allow_expired
-            )
-            token_id = user_info.token_id
-            is_guest = user_info.is_guest
-            shadow_banned = user_info.shadow_banned
-
-            # Deny the request if the user account has expired.
-            if not allow_expired:
-                if await self._account_validity_handler.is_user_expired(
-                    user_info.user_id
-                ):
-                    # Raise the error if either an account validity module has determined
-                    # the account has expired, or the legacy account validity
-                    # implementation is enabled and determined the account has expired
-                    raise AuthError(
-                        403,
-                        "User account has expired",
-                        errcode=Codes.EXPIRED_ACCOUNT,
-                    )
-
-            device_id = user_info.device_id
-
-            if access_token and ip_addr:
+            if ip_addr and (
+                not requester.app_service or self._track_appservice_user_ips
+            ):
+                # XXX(quenting): I'm 95% confident that we could skip setting the
+                # device_id to "dummy-device" for appservices, and that the only impact
+                # would be some rows which whould not deduplicate in the 'user_ips'
+                # table during the transition
+                recorded_device_id = (
+                    "dummy-device"
+                    if requester.device_id is None and requester.app_service is not None
+                    else requester.device_id
+                )
                 await self.store.insert_client_ip(
-                    user_id=user_info.token_owner,
+                    user_id=requester.authenticated_entity,
                     access_token=access_token,
                     ip=ip_addr,
                     user_agent=user_agent,
-                    device_id=device_id,
+                    device_id=recorded_device_id,
                 )
+
                 # Track also the puppeted user client IP if enabled and the user is puppeting
                 if (
-                    user_info.user_id != user_info.token_owner
+                    requester.user.to_string() != requester.authenticated_entity
                     and self._track_puppeted_user_ips
                 ):
                     await self.store.insert_client_ip(
-                        user_id=user_info.user_id,
+                        user_id=requester.user.to_string(),
                         access_token=access_token,
                         ip=ip_addr,
                         user_agent=user_agent,
-                        device_id=device_id,
+                        device_id=requester.device_id,
                     )
 
-            if is_guest and not allow_guest:
+            if requester.is_guest and not allow_guest:
                 raise AuthError(
                     403,
                     "Guest access not allowed",
                     errcode=Codes.GUEST_ACCESS_FORBIDDEN,
                 )
 
-            # Mark the token as used. This is used to invalidate old refresh
-            # tokens after some time.
-            if not user_info.token_used and token_id is not None:
-                await self.store.mark_access_token_as_used(token_id)
-
-            requester = create_requester(
-                user_info.user_id,
-                token_id,
-                is_guest,
-                shadow_banned,
-                device_id,
-                app_service=app_service,
-                authenticated_entity=user_info.token_owner,
-            )
-
             request.requester = requester
             return requester
         except KeyError:
@@ -308,9 +281,7 @@ class Auth:
                 403, "Application service has not registered this user (%s)" % user_id
             )
 
-    async def _get_appservice_user_id_and_device_id(
-        self, request: Request
-    ) -> Tuple[Optional[str], Optional[str], Optional[ApplicationService]]:
+    async def _get_appservice_user(self, request: Request) -> Optional[Requester]:
         """
         Given a request, reads the request parameters to determine:
         - whether it's an application service that's making this request
@@ -325,15 +296,13 @@ class Auth:
              Must use `org.matrix.msc3202.device_id` in place of `device_id` for now.
 
         Returns:
-            3-tuple of
-            (user ID?, device ID?, application service?)
+            the application service `Requester` of that request
 
         Postconditions:
-        - If an application service is returned, so is a user ID
-        - A user ID is never returned without an application service
-        - A device ID is never returned without a user ID or an application service
-        - The returned application service, if present, is permitted to control the
-          returned user ID.
+        - The `app_service` field in the returned `Requester` is set
+        - The `user_id` field in the returned `Requester` is either the application
+          service sender or the controlled user set by the `user_id` URI parameter
+        - The returned application service is permitted to control the returned user ID.
         - The returned device ID, if present, has been checked to be a valid device ID
           for the returned user ID.
         """
@@ -343,12 +312,12 @@ class Auth:
             self.get_access_token_from_request(request)
         )
         if app_service is None:
-            return None, None, None
+            return None
 
         if app_service.ip_range_whitelist:
             ip_address = IPAddress(request.getClientAddress().host)
             if ip_address not in app_service.ip_range_whitelist:
-                return None, None, None
+                return None
 
         # This will always be set by the time Twisted calls us.
         assert request.args is not None
@@ -382,13 +351,15 @@ class Auth:
                     Codes.EXCLUSIVE,
                 )
 
-        return effective_user_id, effective_device_id, app_service
+        return create_requester(
+            effective_user_id, app_service=app_service, device_id=effective_device_id
+        )
 
     async def get_user_by_access_token(
         self,
         token: str,
         allow_expired: bool = False,
-    ) -> TokenLookupResult:
+    ) -> Requester:
         """Validate access token and get user_id from it
 
         Args:
@@ -405,9 +376,9 @@ class Auth:
 
         # First look in the database to see if the access token is present
         # as an opaque token.
-        r = await self.store.get_user_by_access_token(token)
-        if r:
-            valid_until_ms = r.valid_until_ms
+        user_info = await self.store.get_user_by_access_token(token)
+        if user_info:
+            valid_until_ms = user_info.valid_until_ms
             if (
                 not allow_expired
                 and valid_until_ms is not None
@@ -419,7 +390,20 @@ class Auth:
                     msg="Access token has expired", soft_logout=True
                 )
 
-            return r
+            # Mark the token as used. This is used to invalidate old refresh
+            # tokens after some time.
+            await self.store.mark_access_token_as_used(user_info.token_id)
+
+            requester = create_requester(
+                user_id=user_info.user_id,
+                access_token_id=user_info.token_id,
+                is_guest=user_info.is_guest,
+                shadow_banned=user_info.shadow_banned,
+                device_id=user_info.device_id,
+                authenticated_entity=user_info.token_owner,
+            )
+
+            return requester
 
         # If the token isn't found in the database, then it could still be a
         # macaroon for a guest, so we check that here.
@@ -445,11 +429,12 @@ class Auth:
                     "Guest access token used for regular user"
                 )
 
-            return TokenLookupResult(
+            return create_requester(
                 user_id=user_id,
                 is_guest=True,
                 # all guests get the same device id
                 device_id=GUEST_DEVICE_ID,
+                authenticated_entity=user_id,
             )
         except (
             pymacaroons.exceptions.MacaroonException,
@@ -472,32 +457,33 @@ class Auth:
         request.requester = create_requester(service.sender, app_service=service)
         return service
 
-    async def is_server_admin(self, user: UserID) -> bool:
+    async def is_server_admin(self, requester: Requester) -> bool:
         """Check if the given user is a local server admin.
 
         Args:
-            user: user to check
+            requester: The user making the request, according to the access token.
 
         Returns:
             True if the user is an admin
         """
-        return await self.store.is_server_admin(user)
+        return await self.store.is_server_admin(requester.user)
 
-    async def check_can_change_room_list(self, room_id: str, user: UserID) -> bool:
+    async def check_can_change_room_list(
+        self, room_id: str, requester: Requester
+    ) -> bool:
         """Determine whether the user is allowed to edit the room's entry in the
         published room list.
 
         Args:
-            room_id
-            user
+            room_id: The room to check.
+            requester: The user making the request, according to the access token.
         """
 
-        is_admin = await self.is_server_admin(user)
+        is_admin = await self.is_server_admin(requester)
         if is_admin:
             return True
 
-        user_id = user.to_string()
-        await self.check_user_in_room(room_id, user_id)
+        await self.check_user_in_room(room_id, requester)
 
         # We currently require the user is a "moderator" in the room. We do this
         # by checking if they would (theoretically) be able to change the
@@ -516,7 +502,9 @@ class Auth:
         send_level = event_auth.get_send_level(
             EventTypes.CanonicalAlias, "", power_level_event
         )
-        user_level = event_auth.get_user_power_level(user_id, auth_events)
+        user_level = event_auth.get_user_power_level(
+            requester.user.to_string(), auth_events
+        )
 
         return user_level >= send_level
 
@@ -574,16 +562,16 @@ class Auth:
 
     @trace
     async def check_user_in_room_or_world_readable(
-        self, room_id: str, user_id: str, allow_departed_users: bool = False
+        self, room_id: str, requester: Requester, allow_departed_users: bool = False
     ) -> Tuple[str, Optional[str]]:
         """Checks that the user is or was in the room or the room is world
         readable. If it isn't then an exception is raised.
 
         Args:
-            room_id: room to check
-            user_id: user to check
-            allow_departed_users: if True, accept users that were previously
-                members but have now departed
+            room_id: The room to check.
+            requester: The user making the request, according to the access token.
+            allow_departed_users: If True, accept users that were previously
+                members but have now departed.
 
         Returns:
             Resolves to the current membership of the user in the room and the
@@ -598,7 +586,7 @@ class Auth:
             #  * The user is a guest user, and has joined the room
             # else it will throw.
             return await self.check_user_in_room(
-                room_id, user_id, allow_departed_users=allow_departed_users
+                room_id, requester, allow_departed_users=allow_departed_users
             )
         except AuthError:
             visibility = await self._storage_controllers.state.get_current_state_event(
@@ -613,6 +601,6 @@ class Auth:
             raise UnstableSpecAuthError(
                 403,
                 "User %s not in room %s, and room previews are disabled"
-                % (user_id, room_id),
+                % (requester.user, room_id),
                 errcode=Codes.NOT_JOINED,
             )
diff --git a/synapse/handlers/auth.py b/synapse/handlers/auth.py
index bfa553504..0327fc57a 100644
--- a/synapse/handlers/auth.py
+++ b/synapse/handlers/auth.py
@@ -280,7 +280,7 @@ class AuthHandler:
         that it isn't stolen by re-authenticating them.
 
         Args:
-            requester: The user, as given by the access token
+            requester: The user making the request, according to the access token.
 
             request: The request sent by the client.
 
@@ -1435,20 +1435,25 @@ class AuthHandler:
             access_token: access token to be deleted
 
         """
-        user_info = await self.auth.get_user_by_access_token(access_token)
+        token = await self.store.get_user_by_access_token(access_token)
+        if not token:
+            # At this point, the token should already have been fetched once by
+            # the caller, so this should not happen, unless of a race condition
+            # between two delete requests
+            raise SynapseError(HTTPStatus.UNAUTHORIZED, "Unrecognised access token")
         await self.store.delete_access_token(access_token)
 
         # see if any modules want to know about this
         await self.password_auth_provider.on_logged_out(
-            user_id=user_info.user_id,
-            device_id=user_info.device_id,
+            user_id=token.user_id,
+            device_id=token.device_id,
             access_token=access_token,
         )
 
         # delete pushers associated with this access token
-        if user_info.token_id is not None:
+        if token.token_id is not None:
             await self.hs.get_pusherpool().remove_pushers_by_access_token(
-                user_info.user_id, (user_info.token_id,)
+                token.user_id, (token.token_id,)
             )
 
     async def delete_access_tokens_for_user(
diff --git a/synapse/handlers/directory.py b/synapse/handlers/directory.py
index 09a7a4b23..948f66a94 100644
--- a/synapse/handlers/directory.py
+++ b/synapse/handlers/directory.py
@@ -30,7 +30,7 @@ from synapse.api.errors import (
 from synapse.appservice import ApplicationService
 from synapse.module_api import NOT_SPAM
 from synapse.storage.databases.main.directory import RoomAliasMapping
-from synapse.types import JsonDict, Requester, RoomAlias, UserID, get_domain_from_id
+from synapse.types import JsonDict, Requester, RoomAlias, get_domain_from_id
 
 if TYPE_CHECKING:
     from synapse.server import HomeServer
@@ -133,7 +133,7 @@ class DirectoryHandler:
         else:
             # Server admins are not subject to the same constraints as normal
             # users when creating an alias (e.g. being in the room).
-            is_admin = await self.auth.is_server_admin(requester.user)
+            is_admin = await self.auth.is_server_admin(requester)
 
             if (self.require_membership and check_membership) and not is_admin:
                 rooms_for_user = await self.store.get_rooms_for_user(user_id)
@@ -197,7 +197,7 @@ class DirectoryHandler:
         user_id = requester.user.to_string()
 
         try:
-            can_delete = await self._user_can_delete_alias(room_alias, user_id)
+            can_delete = await self._user_can_delete_alias(room_alias, requester)
         except StoreError as e:
             if e.code == 404:
                 raise NotFoundError("Unknown room alias")
@@ -400,7 +400,9 @@ class DirectoryHandler:
         # either no interested services, or no service with an exclusive lock
         return True
 
-    async def _user_can_delete_alias(self, alias: RoomAlias, user_id: str) -> bool:
+    async def _user_can_delete_alias(
+        self, alias: RoomAlias, requester: Requester
+    ) -> bool:
         """Determine whether a user can delete an alias.
 
         One of the following must be true:
@@ -413,7 +415,7 @@ class DirectoryHandler:
         """
         creator = await self.store.get_room_alias_creator(alias.to_string())
 
-        if creator == user_id:
+        if creator == requester.user.to_string():
             return True
 
         # Resolve the alias to the corresponding room.
@@ -422,9 +424,7 @@ class DirectoryHandler:
         if not room_id:
             return False
 
-        return await self.auth.check_can_change_room_list(
-            room_id, UserID.from_string(user_id)
-        )
+        return await self.auth.check_can_change_room_list(room_id, requester)
 
     async def edit_published_room_list(
         self, requester: Requester, room_id: str, visibility: str
@@ -463,7 +463,7 @@ class DirectoryHandler:
             raise SynapseError(400, "Unknown room")
 
         can_change_room_list = await self.auth.check_can_change_room_list(
-            room_id, requester.user
+            room_id, requester
         )
         if not can_change_room_list:
             raise AuthError(
@@ -528,10 +528,8 @@ class DirectoryHandler:
         Get a list of the aliases that currently point to this room on this server
         """
         # allow access to server admins and current members of the room
-        is_admin = await self.auth.is_server_admin(requester.user)
+        is_admin = await self.auth.is_server_admin(requester)
         if not is_admin:
-            await self.auth.check_user_in_room_or_world_readable(
-                room_id, requester.user.to_string()
-            )
+            await self.auth.check_user_in_room_or_world_readable(room_id, requester)
 
         return await self.store.get_aliases_for_room(room_id)
diff --git a/synapse/handlers/initial_sync.py b/synapse/handlers/initial_sync.py
index 6484e47e5..860c82c11 100644
--- a/synapse/handlers/initial_sync.py
+++ b/synapse/handlers/initial_sync.py
@@ -309,18 +309,18 @@ class InitialSyncHandler:
         if blocked:
             raise SynapseError(403, "This room has been blocked on this server")
 
-        user_id = requester.user.to_string()
-
         (
             membership,
             member_event_id,
         ) = await self.auth.check_user_in_room_or_world_readable(
             room_id,
-            user_id,
+            requester,
             allow_departed_users=True,
         )
         is_peeking = member_event_id is None
 
+        user_id = requester.user.to_string()
+
         if membership == Membership.JOIN:
             result = await self._room_initial_sync_joined(
                 user_id, room_id, pagin_config, membership, is_peeking
diff --git a/synapse/handlers/message.py b/synapse/handlers/message.py
index 8f29ee9a8..acd3de06f 100644
--- a/synapse/handlers/message.py
+++ b/synapse/handlers/message.py
@@ -104,7 +104,7 @@ class MessageHandler:
 
     async def get_room_data(
         self,
-        user_id: str,
+        requester: Requester,
         room_id: str,
         event_type: str,
         state_key: str,
@@ -112,7 +112,7 @@ class MessageHandler:
         """Get data from a room.
 
         Args:
-            user_id
+            requester: The user who did the request.
             room_id
             event_type
             state_key
@@ -125,7 +125,7 @@ class MessageHandler:
             membership,
             membership_event_id,
         ) = await self.auth.check_user_in_room_or_world_readable(
-            room_id, user_id, allow_departed_users=True
+            room_id, requester, allow_departed_users=True
         )
 
         if membership == Membership.JOIN:
@@ -161,11 +161,10 @@ class MessageHandler:
 
     async def get_state_events(
         self,
-        user_id: str,
+        requester: Requester,
         room_id: str,
         state_filter: Optional[StateFilter] = None,
         at_token: Optional[StreamToken] = None,
-        is_guest: bool = False,
     ) -> List[dict]:
         """Retrieve all state events for a given room. If the user is
         joined to the room then return the current state. If the user has
@@ -174,14 +173,13 @@ class MessageHandler:
         visible.
 
         Args:
-            user_id: The user requesting state events.
+            requester: The user requesting state events.
             room_id: The room ID to get all state events from.
             state_filter: The state filter used to fetch state from the database.
             at_token: the stream token of the at which we are requesting
                 the stats. If the user is not allowed to view the state as of that
                 stream token, we raise a 403 SynapseError. If None, returns the current
                 state based on the current_state_events table.
-            is_guest: whether this user is a guest
         Returns:
             A list of dicts representing state events. [{}, {}, {}]
         Raises:
@@ -191,6 +189,7 @@ class MessageHandler:
             members of this room.
         """
         state_filter = state_filter or StateFilter.all()
+        user_id = requester.user.to_string()
 
         if at_token:
             last_event_id = (
@@ -223,7 +222,7 @@ class MessageHandler:
                 membership,
                 membership_event_id,
             ) = await self.auth.check_user_in_room_or_world_readable(
-                room_id, user_id, allow_departed_users=True
+                room_id, requester, allow_departed_users=True
             )
 
             if membership == Membership.JOIN:
@@ -317,12 +316,11 @@ class MessageHandler:
         Returns:
             A dict of user_id to profile info
         """
-        user_id = requester.user.to_string()
         if not requester.app_service:
             # We check AS auth after fetching the room membership, as it
             # requires us to pull out all joined members anyway.
             membership, _ = await self.auth.check_user_in_room_or_world_readable(
-                room_id, user_id, allow_departed_users=True
+                room_id, requester, allow_departed_users=True
             )
             if membership != Membership.JOIN:
                 raise SynapseError(
@@ -340,7 +338,10 @@ class MessageHandler:
         # If this is an AS, double check that they are allowed to see the members.
         # This can either be because the AS user is in the room or because there
         # is a user in the room that the AS is "interested in"
-        if requester.app_service and user_id not in users_with_profile:
+        if (
+            requester.app_service
+            and requester.user.to_string() not in users_with_profile
+        ):
             for uid in users_with_profile:
                 if requester.app_service.is_interested_in_user(uid):
                     break
diff --git a/synapse/handlers/pagination.py b/synapse/handlers/pagination.py
index e1e34e3b1..74e944bce 100644
--- a/synapse/handlers/pagination.py
+++ b/synapse/handlers/pagination.py
@@ -464,7 +464,7 @@ class PaginationHandler:
                 membership,
                 member_event_id,
             ) = await self.auth.check_user_in_room_or_world_readable(
-                room_id, user_id, allow_departed_users=True
+                room_id, requester, allow_departed_users=True
             )
 
             if pagin_config.direction == "b":
diff --git a/synapse/handlers/register.py b/synapse/handlers/register.py
index c77d18172..20ec22105 100644
--- a/synapse/handlers/register.py
+++ b/synapse/handlers/register.py
@@ -29,7 +29,13 @@ from synapse.api.constants import (
     JoinRules,
     LoginType,
 )
-from synapse.api.errors import AuthError, Codes, ConsentNotGivenError, SynapseError
+from synapse.api.errors import (
+    AuthError,
+    Codes,
+    ConsentNotGivenError,
+    InvalidClientTokenError,
+    SynapseError,
+)
 from synapse.appservice import ApplicationService
 from synapse.config.server import is_threepid_reserved
 from synapse.http.servlet import assert_params_in_dict
@@ -180,10 +186,7 @@ class RegistrationHandler:
                 )
             if guest_access_token:
                 user_data = await self.auth.get_user_by_access_token(guest_access_token)
-                if (
-                    not user_data.is_guest
-                    or UserID.from_string(user_data.user_id).localpart != localpart
-                ):
+                if not user_data.is_guest or user_data.user.localpart != localpart:
                     raise AuthError(
                         403,
                         "Cannot register taken user ID without valid guest "
@@ -618,7 +621,7 @@ class RegistrationHandler:
         user_id = user.to_string()
         service = self.store.get_app_service_by_token(as_token)
         if not service:
-            raise AuthError(403, "Invalid application service token.")
+            raise InvalidClientTokenError()
         if not service.is_interested_in_user(user_id):
             raise SynapseError(
                 400,
diff --git a/synapse/handlers/relations.py b/synapse/handlers/relations.py
index 72d25df8c..28d7093f0 100644
--- a/synapse/handlers/relations.py
+++ b/synapse/handlers/relations.py
@@ -103,7 +103,7 @@ class RelationsHandler:
 
         # TODO Properly handle a user leaving a room.
         (_, member_event_id) = await self._auth.check_user_in_room_or_world_readable(
-            room_id, user_id, allow_departed_users=True
+            room_id, requester, allow_departed_users=True
         )
 
         # This gets the original event and checks that a) the event exists and
diff --git a/synapse/handlers/room.py b/synapse/handlers/room.py
index 55395457c..2bf0ebd02 100644
--- a/synapse/handlers/room.py
+++ b/synapse/handlers/room.py
@@ -721,7 +721,7 @@ class RoomCreationHandler:
             # allow the server notices mxid to create rooms
             is_requester_admin = True
         else:
-            is_requester_admin = await self.auth.is_server_admin(requester.user)
+            is_requester_admin = await self.auth.is_server_admin(requester)
 
         # Let the third party rules modify the room creation config if needed, or abort
         # the room creation entirely with an exception.
@@ -1279,7 +1279,7 @@ class RoomContextHandler:
         """
         user = requester.user
         if use_admin_priviledge:
-            await assert_user_is_admin(self.auth, requester.user)
+            await assert_user_is_admin(self.auth, requester)
 
         before_limit = math.floor(limit / 2.0)
         after_limit = limit - before_limit
diff --git a/synapse/handlers/room_member.py b/synapse/handlers/room_member.py
index 70dc69c80..d1909665d 100644
--- a/synapse/handlers/room_member.py
+++ b/synapse/handlers/room_member.py
@@ -179,7 +179,7 @@ class RoomMemberHandler(metaclass=abc.ABCMeta):
         """Try and join a room that this server is not in
 
         Args:
-            requester
+            requester: The user making the request, according to the access token.
             remote_room_hosts: List of servers that can be used to join via.
             room_id: Room that we are trying to join
             user: User who is trying to join
@@ -744,7 +744,7 @@ class RoomMemberHandler(metaclass=abc.ABCMeta):
                 is_requester_admin = True
 
             else:
-                is_requester_admin = await self.auth.is_server_admin(requester.user)
+                is_requester_admin = await self.auth.is_server_admin(requester)
 
             if not is_requester_admin:
                 if self.config.server.block_non_admin_invites:
@@ -868,7 +868,7 @@ class RoomMemberHandler(metaclass=abc.ABCMeta):
                 bypass_spam_checker = True
 
             else:
-                bypass_spam_checker = await self.auth.is_server_admin(requester.user)
+                bypass_spam_checker = await self.auth.is_server_admin(requester)
 
             inviter = await self._get_inviter(target.to_string(), room_id)
             if (
@@ -1410,7 +1410,7 @@ class RoomMemberHandler(metaclass=abc.ABCMeta):
             ShadowBanError if the requester has been shadow-banned.
         """
         if self.config.server.block_non_admin_invites:
-            is_requester_admin = await self.auth.is_server_admin(requester.user)
+            is_requester_admin = await self.auth.is_server_admin(requester)
             if not is_requester_admin:
                 raise SynapseError(
                     403, "Invites have been disabled on this server", Codes.FORBIDDEN
@@ -1693,7 +1693,7 @@ class RoomMemberMasterHandler(RoomMemberHandler):
             check_complexity
             and self.hs.config.server.limit_remote_rooms.admins_can_join
         ):
-            check_complexity = not await self.auth.is_server_admin(user)
+            check_complexity = not await self.store.is_server_admin(user)
 
         if check_complexity:
             # Fetch the room complexity
diff --git a/synapse/handlers/typing.py b/synapse/handlers/typing.py
index 27aa0d312..bcac3372a 100644
--- a/synapse/handlers/typing.py
+++ b/synapse/handlers/typing.py
@@ -253,12 +253,11 @@ class TypingWriterHandler(FollowerTypingHandler):
         self, target_user: UserID, requester: Requester, room_id: str, timeout: int
     ) -> None:
         target_user_id = target_user.to_string()
-        auth_user_id = requester.user.to_string()
 
         if not self.is_mine_id(target_user_id):
             raise SynapseError(400, "User is not hosted on this homeserver")
 
-        if target_user_id != auth_user_id:
+        if target_user != requester.user:
             raise AuthError(400, "Cannot set another user's typing state")
 
         if requester.shadow_banned:
@@ -266,7 +265,7 @@ class TypingWriterHandler(FollowerTypingHandler):
             await self.clock.sleep(random.randint(1, 10))
             raise ShadowBanError()
 
-        await self.auth.check_user_in_room(room_id, target_user_id)
+        await self.auth.check_user_in_room(room_id, requester)
 
         logger.debug("%s has started typing in %s", target_user_id, room_id)
 
@@ -289,12 +288,11 @@ class TypingWriterHandler(FollowerTypingHandler):
         self, target_user: UserID, requester: Requester, room_id: str
     ) -> None:
         target_user_id = target_user.to_string()
-        auth_user_id = requester.user.to_string()
 
         if not self.is_mine_id(target_user_id):
             raise SynapseError(400, "User is not hosted on this homeserver")
 
-        if target_user_id != auth_user_id:
+        if target_user != requester.user:
             raise AuthError(400, "Cannot set another user's typing state")
 
         if requester.shadow_banned:
@@ -302,7 +300,7 @@ class TypingWriterHandler(FollowerTypingHandler):
             await self.clock.sleep(random.randint(1, 10))
             raise ShadowBanError()
 
-        await self.auth.check_user_in_room(room_id, target_user_id)
+        await self.auth.check_user_in_room(room_id, requester)
 
         logger.debug("%s has stopped typing in %s", target_user_id, room_id)
 
diff --git a/synapse/http/site.py b/synapse/http/site.py
index eeec74b78..1155f3f61 100644
--- a/synapse/http/site.py
+++ b/synapse/http/site.py
@@ -226,7 +226,7 @@ class SynapseRequest(Request):
 
             # If this is a request where the target user doesn't match the user who
             # authenticated (e.g. and admin is puppetting a user) then we return both.
-            if self._requester.user.to_string() != authenticated_entity:
+            if requester != authenticated_entity:
                 return requester, authenticated_entity
 
             return requester, None
diff --git a/synapse/rest/admin/_base.py b/synapse/rest/admin/_base.py
index 399b205aa..b467a61df 100644
--- a/synapse/rest/admin/_base.py
+++ b/synapse/rest/admin/_base.py
@@ -19,7 +19,7 @@ from typing import Iterable, Pattern
 from synapse.api.auth import Auth
 from synapse.api.errors import AuthError
 from synapse.http.site import SynapseRequest
-from synapse.types import UserID
+from synapse.types import Requester
 
 
 def admin_patterns(path_regex: str, version: str = "v1") -> Iterable[Pattern]:
@@ -48,19 +48,19 @@ async def assert_requester_is_admin(auth: Auth, request: SynapseRequest) -> None
         AuthError if the requester is not a server admin
     """
     requester = await auth.get_user_by_req(request)
-    await assert_user_is_admin(auth, requester.user)
+    await assert_user_is_admin(auth, requester)
 
 
-async def assert_user_is_admin(auth: Auth, user_id: UserID) -> None:
+async def assert_user_is_admin(auth: Auth, requester: Requester) -> None:
     """Verify that the given user is an admin user
 
     Args:
         auth: Auth singleton
-        user_id: user to check
+        requester: The user making the request, according to the access token.
 
     Raises:
         AuthError if the user is not a server admin
     """
-    is_admin = await auth.is_server_admin(user_id)
+    is_admin = await auth.is_server_admin(requester)
     if not is_admin:
         raise AuthError(HTTPStatus.FORBIDDEN, "You are not a server admin")
diff --git a/synapse/rest/admin/media.py b/synapse/rest/admin/media.py
index 19d4a008e..73470f09a 100644
--- a/synapse/rest/admin/media.py
+++ b/synapse/rest/admin/media.py
@@ -54,7 +54,7 @@ class QuarantineMediaInRoom(RestServlet):
         self, request: SynapseRequest, room_id: str
     ) -> Tuple[int, JsonDict]:
         requester = await self.auth.get_user_by_req(request)
-        await assert_user_is_admin(self.auth, requester.user)
+        await assert_user_is_admin(self.auth, requester)
 
         logging.info("Quarantining room: %s", room_id)
 
@@ -81,7 +81,7 @@ class QuarantineMediaByUser(RestServlet):
         self, request: SynapseRequest, user_id: str
     ) -> Tuple[int, JsonDict]:
         requester = await self.auth.get_user_by_req(request)
-        await assert_user_is_admin(self.auth, requester.user)
+        await assert_user_is_admin(self.auth, requester)
 
         logging.info("Quarantining media by user: %s", user_id)
 
@@ -110,7 +110,7 @@ class QuarantineMediaByID(RestServlet):
         self, request: SynapseRequest, server_name: str, media_id: str
     ) -> Tuple[int, JsonDict]:
         requester = await self.auth.get_user_by_req(request)
-        await assert_user_is_admin(self.auth, requester.user)
+        await assert_user_is_admin(self.auth, requester)
 
         logging.info("Quarantining media by ID: %s/%s", server_name, media_id)
 
diff --git a/synapse/rest/admin/rooms.py b/synapse/rest/admin/rooms.py
index 68054ffc2..3d870629c 100644
--- a/synapse/rest/admin/rooms.py
+++ b/synapse/rest/admin/rooms.py
@@ -75,7 +75,7 @@ class RoomRestV2Servlet(RestServlet):
     ) -> Tuple[int, JsonDict]:
 
         requester = await self._auth.get_user_by_req(request)
-        await assert_user_is_admin(self._auth, requester.user)
+        await assert_user_is_admin(self._auth, requester)
 
         content = parse_json_object_from_request(request)
 
@@ -327,7 +327,7 @@ class RoomRestServlet(RestServlet):
         pagination_handler: "PaginationHandler",
     ) -> Tuple[int, JsonDict]:
         requester = await auth.get_user_by_req(request)
-        await assert_user_is_admin(auth, requester.user)
+        await assert_user_is_admin(auth, requester)
 
         content = parse_json_object_from_request(request)
 
@@ -461,7 +461,7 @@ class JoinRoomAliasServlet(ResolveRoomIdMixin, RestServlet):
         assert request.args is not None
 
         requester = await self.auth.get_user_by_req(request)
-        await assert_user_is_admin(self.auth, requester.user)
+        await assert_user_is_admin(self.auth, requester)
 
         content = parse_json_object_from_request(request)
 
@@ -551,7 +551,7 @@ class MakeRoomAdminRestServlet(ResolveRoomIdMixin, RestServlet):
         self, request: SynapseRequest, room_identifier: str
     ) -> Tuple[int, JsonDict]:
         requester = await self.auth.get_user_by_req(request)
-        await assert_user_is_admin(self.auth, requester.user)
+        await assert_user_is_admin(self.auth, requester)
         content = parse_json_object_from_request(request, allow_empty_body=True)
 
         room_id, _ = await self.resolve_room_id(room_identifier)
@@ -742,7 +742,7 @@ class RoomEventContextServlet(RestServlet):
         self, request: SynapseRequest, room_id: str, event_id: str
     ) -> Tuple[int, JsonDict]:
         requester = await self.auth.get_user_by_req(request, allow_guest=False)
-        await assert_user_is_admin(self.auth, requester.user)
+        await assert_user_is_admin(self.auth, requester)
 
         limit = parse_integer(request, "limit", default=10)
 
@@ -834,7 +834,7 @@ class BlockRoomRestServlet(RestServlet):
         self, request: SynapseRequest, room_id: str
     ) -> Tuple[int, JsonDict]:
         requester = await self._auth.get_user_by_req(request)
-        await assert_user_is_admin(self._auth, requester.user)
+        await assert_user_is_admin(self._auth, requester)
 
         content = parse_json_object_from_request(request)
 
diff --git a/synapse/rest/admin/users.py b/synapse/rest/admin/users.py
index ba2f7fa6d..78ee9b653 100644
--- a/synapse/rest/admin/users.py
+++ b/synapse/rest/admin/users.py
@@ -183,7 +183,7 @@ class UserRestServletV2(RestServlet):
         self, request: SynapseRequest, user_id: str
     ) -> Tuple[int, JsonDict]:
         requester = await self.auth.get_user_by_req(request)
-        await assert_user_is_admin(self.auth, requester.user)
+        await assert_user_is_admin(self.auth, requester)
 
         target_user = UserID.from_string(user_id)
         body = parse_json_object_from_request(request)
@@ -575,10 +575,9 @@ class WhoisRestServlet(RestServlet):
     ) -> Tuple[int, JsonDict]:
         target_user = UserID.from_string(user_id)
         requester = await self.auth.get_user_by_req(request)
-        auth_user = requester.user
 
-        if target_user != auth_user:
-            await assert_user_is_admin(self.auth, auth_user)
+        if target_user != requester.user:
+            await assert_user_is_admin(self.auth, requester)
 
         if not self.is_mine(target_user):
             raise SynapseError(HTTPStatus.BAD_REQUEST, "Can only whois a local user")
@@ -601,7 +600,7 @@ class DeactivateAccountRestServlet(RestServlet):
         self, request: SynapseRequest, target_user_id: str
     ) -> Tuple[int, JsonDict]:
         requester = await self.auth.get_user_by_req(request)
-        await assert_user_is_admin(self.auth, requester.user)
+        await assert_user_is_admin(self.auth, requester)
 
         if not self.is_mine(UserID.from_string(target_user_id)):
             raise SynapseError(
@@ -693,7 +692,7 @@ class ResetPasswordRestServlet(RestServlet):
         This needs user to have administrator access in Synapse.
         """
         requester = await self.auth.get_user_by_req(request)
-        await assert_user_is_admin(self.auth, requester.user)
+        await assert_user_is_admin(self.auth, requester)
 
         UserID.from_string(target_user_id)
 
@@ -807,7 +806,7 @@ class UserAdminServlet(RestServlet):
         self, request: SynapseRequest, user_id: str
     ) -> Tuple[int, JsonDict]:
         requester = await self.auth.get_user_by_req(request)
-        await assert_user_is_admin(self.auth, requester.user)
+        await assert_user_is_admin(self.auth, requester)
         auth_user = requester.user
 
         target_user = UserID.from_string(user_id)
@@ -921,7 +920,7 @@ class UserTokenRestServlet(RestServlet):
         self, request: SynapseRequest, user_id: str
     ) -> Tuple[int, JsonDict]:
         requester = await self.auth.get_user_by_req(request)
-        await assert_user_is_admin(self.auth, requester.user)
+        await assert_user_is_admin(self.auth, requester)
         auth_user = requester.user
 
         if not self.is_mine_id(user_id):
diff --git a/synapse/rest/client/profile.py b/synapse/rest/client/profile.py
index c16d70790..e69fa0829 100644
--- a/synapse/rest/client/profile.py
+++ b/synapse/rest/client/profile.py
@@ -66,7 +66,7 @@ class ProfileDisplaynameRestServlet(RestServlet):
     ) -> Tuple[int, JsonDict]:
         requester = await self.auth.get_user_by_req(request, allow_guest=True)
         user = UserID.from_string(user_id)
-        is_admin = await self.auth.is_server_admin(requester.user)
+        is_admin = await self.auth.is_server_admin(requester)
 
         content = parse_json_object_from_request(request)
 
@@ -123,7 +123,7 @@ class ProfileAvatarURLRestServlet(RestServlet):
     ) -> Tuple[int, JsonDict]:
         requester = await self.auth.get_user_by_req(request)
         user = UserID.from_string(user_id)
-        is_admin = await self.auth.is_server_admin(requester.user)
+        is_admin = await self.auth.is_server_admin(requester)
 
         content = parse_json_object_from_request(request)
         try:
diff --git a/synapse/rest/client/register.py b/synapse/rest/client/register.py
index 956c45e60..1b953d3fa 100644
--- a/synapse/rest/client/register.py
+++ b/synapse/rest/client/register.py
@@ -484,9 +484,6 @@ class RegisterRestServlet(RestServlet):
                     "Appservice token must be provided when using a type of m.login.application_service",
                 )
 
-            # Verify the AS
-            self.auth.get_appservice_by_req(request)
-
             # Set the desired user according to the AS API (which uses the
             # 'user' key not 'username'). Since this is a new addition, we'll
             # fallback to 'username' if they gave one.
diff --git a/synapse/rest/client/room.py b/synapse/rest/client/room.py
index 13bc9482c..0eafbae45 100644
--- a/synapse/rest/client/room.py
+++ b/synapse/rest/client/room.py
@@ -229,7 +229,7 @@ class RoomStateEventRestServlet(TransactionRestServlet):
 
         msg_handler = self.message_handler
         data = await msg_handler.get_room_data(
-            user_id=requester.user.to_string(),
+            requester=requester,
             room_id=room_id,
             event_type=event_type,
             state_key=state_key,
@@ -574,7 +574,7 @@ class RoomMemberListRestServlet(RestServlet):
 
         events = await handler.get_state_events(
             room_id=room_id,
-            user_id=requester.user.to_string(),
+            requester=requester,
             at_token=at_token,
             state_filter=StateFilter.from_types([(EventTypes.Member, None)]),
         )
@@ -696,8 +696,7 @@ class RoomStateRestServlet(RestServlet):
         # Get all the current state for this room
         events = await self.message_handler.get_state_events(
             room_id=room_id,
-            user_id=requester.user.to_string(),
-            is_guest=requester.is_guest,
+            requester=requester,
         )
         return 200, events
 
@@ -755,7 +754,7 @@ class RoomEventServlet(RestServlet):
             == "true"
         )
         if include_unredacted_content and not await self.auth.is_server_admin(
-            requester.user
+            requester
         ):
             power_level_event = (
                 await self._storage_controllers.state.get_current_state_event(
@@ -1260,9 +1259,7 @@ class TimestampLookupRestServlet(RestServlet):
         self, request: SynapseRequest, room_id: str
     ) -> Tuple[int, JsonDict]:
         requester = await self._auth.get_user_by_req(request)
-        await self._auth.check_user_in_room_or_world_readable(
-            room_id, requester.user.to_string()
-        )
+        await self._auth.check_user_in_room_or_world_readable(room_id, requester)
 
         timestamp = parse_integer(request, "ts", required=True)
         direction = parse_string(request, "dir", default="f", allowed_values=["f", "b"])
diff --git a/synapse/server_notices/server_notices_manager.py b/synapse/server_notices/server_notices_manager.py
index 8ecab86ec..70d054a8f 100644
--- a/synapse/server_notices/server_notices_manager.py
+++ b/synapse/server_notices/server_notices_manager.py
@@ -244,7 +244,7 @@ class ServerNoticesManager:
         assert self.server_notices_mxid is not None
 
         notice_user_data_in_room = await self._message_handler.get_room_data(
-            self.server_notices_mxid,
+            create_requester(self.server_notices_mxid),
             room_id,
             EventTypes.Member,
             self.server_notices_mxid,
diff --git a/synapse/storage/databases/main/registration.py b/synapse/storage/databases/main/registration.py
index cb63cd9b7..7fb9c801d 100644
--- a/synapse/storage/databases/main/registration.py
+++ b/synapse/storage/databases/main/registration.py
@@ -69,9 +69,9 @@ class TokenLookupResult:
     """
 
     user_id: str
+    token_id: int
     is_guest: bool = False
     shadow_banned: bool = False
-    token_id: Optional[int] = None
     device_id: Optional[str] = None
     valid_until_ms: Optional[int] = None
     token_owner: str = attr.ib()
diff --git a/tests/api/test_auth.py b/tests/api/test_auth.py
index dfcfaf79b..e0f363555 100644
--- a/tests/api/test_auth.py
+++ b/tests/api/test_auth.py
@@ -284,10 +284,13 @@ class AuthTestCase(unittest.HomeserverTestCase):
             TokenLookupResult(
                 user_id="@baldrick:matrix.org",
                 device_id="device",
+                token_id=5,
                 token_owner="@admin:matrix.org",
+                token_used=True,
             )
         )
         self.store.insert_client_ip = simple_async_mock(None)
+        self.store.mark_access_token_as_used = simple_async_mock(None)
         request = Mock(args={})
         request.getClientAddress.return_value.host = "127.0.0.1"
         request.args[b"access_token"] = [self.test_token]
@@ -301,10 +304,13 @@ class AuthTestCase(unittest.HomeserverTestCase):
             TokenLookupResult(
                 user_id="@baldrick:matrix.org",
                 device_id="device",
+                token_id=5,
                 token_owner="@admin:matrix.org",
+                token_used=True,
             )
         )
         self.store.insert_client_ip = simple_async_mock(None)
+        self.store.mark_access_token_as_used = simple_async_mock(None)
         request = Mock(args={})
         request.getClientAddress.return_value.host = "127.0.0.1"
         request.args[b"access_token"] = [self.test_token]
@@ -347,7 +353,7 @@ class AuthTestCase(unittest.HomeserverTestCase):
         serialized = macaroon.serialize()
 
         user_info = self.get_success(self.auth.get_user_by_access_token(serialized))
-        self.assertEqual(user_id, user_info.user_id)
+        self.assertEqual(user_id, user_info.user.to_string())
         self.assertTrue(user_info.is_guest)
         self.store.get_user_by_id.assert_called_with(user_id)
 
diff --git a/tests/handlers/test_typing.py b/tests/handlers/test_typing.py
index 7af133312..8adba29d7 100644
--- a/tests/handlers/test_typing.py
+++ b/tests/handlers/test_typing.py
@@ -25,7 +25,7 @@ from synapse.api.constants import EduTypes
 from synapse.api.errors import AuthError
 from synapse.federation.transport.server import TransportLayerServer
 from synapse.server import HomeServer
-from synapse.types import JsonDict, UserID, create_requester
+from synapse.types import JsonDict, Requester, UserID, create_requester
 from synapse.util import Clock
 
 from tests import unittest
@@ -117,8 +117,10 @@ class TypingNotificationsTestCase(unittest.HomeserverTestCase):
 
         self.room_members = []
 
-        async def check_user_in_room(room_id: str, user_id: str) -> None:
-            if user_id not in [u.to_string() for u in self.room_members]:
+        async def check_user_in_room(room_id: str, requester: Requester) -> None:
+            if requester.user.to_string() not in [
+                u.to_string() for u in self.room_members
+            ]:
                 raise AuthError(401, "User is not in the room")
             return None
 
diff --git a/tests/rest/client/test_retention.py b/tests/rest/client/test_retention.py
index ac9c11335..9c8c1889d 100644
--- a/tests/rest/client/test_retention.py
+++ b/tests/rest/client/test_retention.py
@@ -20,7 +20,7 @@ from synapse.api.constants import EventTypes
 from synapse.rest import admin
 from synapse.rest.client import login, room
 from synapse.server import HomeServer
-from synapse.types import JsonDict
+from synapse.types import JsonDict, create_requester
 from synapse.util import Clock
 from synapse.visibility import filter_events_for_client
 
@@ -188,7 +188,7 @@ class RetentionTestCase(unittest.HomeserverTestCase):
         message_handler = self.hs.get_message_handler()
         create_event = self.get_success(
             message_handler.get_room_data(
-                self.user_id, room_id, EventTypes.Create, state_key=""
+                create_requester(self.user_id), room_id, EventTypes.Create, state_key=""
             )
         )
 
diff --git a/tests/rest/client/test_shadow_banned.py b/tests/rest/client/test_shadow_banned.py
index d9bd8c4a2..c50f034b3 100644
--- a/tests/rest/client/test_shadow_banned.py
+++ b/tests/rest/client/test_shadow_banned.py
@@ -26,7 +26,7 @@ from synapse.rest.client import (
     room_upgrade_rest_servlet,
 )
 from synapse.server import HomeServer
-from synapse.types import UserID
+from synapse.types import UserID, create_requester
 from synapse.util import Clock
 
 from tests import unittest
@@ -275,7 +275,7 @@ class ProfileTestCase(_ShadowBannedBase):
         message_handler = self.hs.get_message_handler()
         event = self.get_success(
             message_handler.get_room_data(
-                self.banned_user_id,
+                create_requester(self.banned_user_id),
                 room_id,
                 "m.room.member",
                 self.banned_user_id,
@@ -310,7 +310,7 @@ class ProfileTestCase(_ShadowBannedBase):
         message_handler = self.hs.get_message_handler()
         event = self.get_success(
             message_handler.get_room_data(
-                self.banned_user_id,
+                create_requester(self.banned_user_id),
                 room_id,
                 "m.room.member",
                 self.banned_user_id,