diff --git a/changelog.d/10447.feature b/changelog.d/10447.feature
new file mode 100644
index 000000000..df8bb5116
--- /dev/null
+++ b/changelog.d/10447.feature
@@ -0,0 +1 @@
+Update support for [MSC3083](https://github.com/matrix-org/matrix-doc/pull/3083) to consider changes in the MSC around which servers can issue join events.
diff --git a/synapse/federation/federation_client.py b/synapse/federation/federation_client.py
index dbadf102f..b7a10da15 100644
--- a/synapse/federation/federation_client.py
+++ b/synapse/federation/federation_client.py
@@ -22,6 +22,7 @@ from typing import (
     Awaitable,
     Callable,
     Collection,
+    Container,
     Dict,
     Iterable,
     List,
@@ -513,6 +514,7 @@ class FederationClient(FederationBase):
         description: str,
         destinations: Iterable[str],
         callback: Callable[[str], Awaitable[T]],
+        failover_errcodes: Optional[Container[str]] = None,
         failover_on_unknown_endpoint: bool = False,
     ) -> T:
         """Try an operation on a series of servers, until it succeeds
@@ -533,6 +535,9 @@ class FederationClient(FederationBase):
                 next server tried. Normally the stacktrace is logged but this is
                 suppressed if the exception is an InvalidResponseError.
 
+            failover_errcodes: Error codes (specific to this endpoint) which should
+                cause a failover when received as part of an HTTP 400 error.
+
             failover_on_unknown_endpoint: if True, we will try other servers if it looks
                 like a server doesn't support the endpoint. This is typically useful
                 if the endpoint in question is new or experimental.
@@ -544,6 +549,9 @@ class FederationClient(FederationBase):
             SynapseError if the chosen remote server returns a 300/400 code, or
             no servers were reachable.
         """
+        if failover_errcodes is None:
+            failover_errcodes = ()
+
         for destination in destinations:
             if destination == self.server_name:
                 continue
@@ -558,11 +566,17 @@ class FederationClient(FederationBase):
                 synapse_error = e.to_synapse_error()
                 failover = False
 
-                # Failover on an internal server error, or if the destination
-                # doesn't implemented the endpoint for some reason.
+                # Failover should occur:
+                #
+                # * On internal server errors.
+                # * If the destination responds that it cannot complete the request.
+                # * If the destination doesn't implemented the endpoint for some reason.
                 if 500 <= e.code < 600:
                     failover = True
 
+                elif e.code == 400 and synapse_error.errcode in failover_errcodes:
+                    failover = True
+
                 elif failover_on_unknown_endpoint and self._is_unknown_endpoint(
                     e, synapse_error
                 ):
@@ -678,8 +692,20 @@ class FederationClient(FederationBase):
 
             return destination, ev, room_version
 
+        # MSC3083 defines additional error codes for room joins. Unfortunately
+        # we do not yet know the room version, assume these will only be returned
+        # by valid room versions.
+        failover_errcodes = (
+            (Codes.UNABLE_AUTHORISE_JOIN, Codes.UNABLE_TO_GRANT_JOIN)
+            if membership == Membership.JOIN
+            else None
+        )
+
         return await self._try_destination_list(
-            "make_" + membership, destinations, send_request
+            "make_" + membership,
+            destinations,
+            send_request,
+            failover_errcodes=failover_errcodes,
         )
 
     async def send_join(
@@ -818,7 +844,14 @@ class FederationClient(FederationBase):
                 origin=destination,
             )
 
+        # MSC3083 defines additional error codes for room joins.
+        failover_errcodes = None
         if room_version.msc3083_join_rules:
+            failover_errcodes = (
+                Codes.UNABLE_AUTHORISE_JOIN,
+                Codes.UNABLE_TO_GRANT_JOIN,
+            )
+
             # If the join is being authorised via allow rules, we need to send
             # the /send_join back to the same server that was originally used
             # with /make_join.
@@ -827,7 +860,9 @@ class FederationClient(FederationBase):
                     get_domain_from_id(pdu.content["join_authorised_via_users_server"])
                 ]
 
-        return await self._try_destination_list("send_join", destinations, send_request)
+        return await self._try_destination_list(
+            "send_join", destinations, send_request, failover_errcodes=failover_errcodes
+        )
 
     async def _do_send_join(
         self, room_version: RoomVersion, destination: str, pdu: EventBase