diff --git a/synapse/api/urls.py b/synapse/api/urls.py
index f78695b65..ba019001f 100644
--- a/synapse/api/urls.py
+++ b/synapse/api/urls.py
@@ -24,7 +24,8 @@ from synapse.config import ConfigError
 
 CLIENT_PREFIX = "/_matrix/client/api/v1"
 CLIENT_V2_ALPHA_PREFIX = "/_matrix/client/v2_alpha"
-FEDERATION_PREFIX = "/_matrix/federation/v1"
+FEDERATION_PREFIX = "/_matrix/federation"
+FEDERATION_V1_PREFIX = FEDERATION_PREFIX + "/v1"
 STATIC_PREFIX = "/_matrix/static"
 WEB_CLIENT_PREFIX = "/_matrix/client"
 CONTENT_REPO_PREFIX = "/_matrix/content"
diff --git a/synapse/federation/transport/client.py b/synapse/federation/transport/client.py
index edba5a980..260178c47 100644
--- a/synapse/federation/transport/client.py
+++ b/synapse/federation/transport/client.py
@@ -21,7 +21,7 @@ from six.moves import urllib
 from twisted.internet import defer
 
 from synapse.api.constants import Membership
-from synapse.api.urls import FEDERATION_PREFIX as PREFIX
+from synapse.api.urls import FEDERATION_V1_PREFIX
 from synapse.util.logutils import log_function
 
 logger = logging.getLogger(__name__)
@@ -51,7 +51,7 @@ class TransportLayerClient(object):
         logger.debug("get_room_state dest=%s, room=%s",
                      destination, room_id)
 
-        path = _create_path(PREFIX, "/state/%s/", room_id)
+        path = _create_v1_path("/state/%s/", room_id)
         return self.client.get_json(
             destination, path=path, args={"event_id": event_id},
         )
@@ -73,7 +73,7 @@ class TransportLayerClient(object):
         logger.debug("get_room_state_ids dest=%s, room=%s",
                      destination, room_id)
 
-        path = _create_path(PREFIX, "/state_ids/%s/", room_id)
+        path = _create_v1_path("/state_ids/%s/", room_id)
         return self.client.get_json(
             destination, path=path, args={"event_id": event_id},
         )
@@ -95,7 +95,7 @@ class TransportLayerClient(object):
         logger.debug("get_pdu dest=%s, event_id=%s",
                      destination, event_id)
 
-        path = _create_path(PREFIX, "/event/%s/", event_id)
+        path = _create_v1_path("/event/%s/", event_id)
         return self.client.get_json(destination, path=path, timeout=timeout)
 
     @log_function
@@ -121,7 +121,7 @@ class TransportLayerClient(object):
             # TODO: raise?
             return
 
-        path = _create_path(PREFIX, "/backfill/%s/", room_id)
+        path = _create_v1_path("/backfill/%s/", room_id)
 
         args = {
             "v": event_tuples,
@@ -167,7 +167,7 @@ class TransportLayerClient(object):
         # generated by the json_data_callback.
         json_data = transaction.get_dict()
 
-        path = _create_path(PREFIX, "/send/%s/", transaction.transaction_id)
+        path = _create_v1_path("/send/%s/", transaction.transaction_id)
 
         response = yield self.client.put_json(
             transaction.destination,
@@ -184,7 +184,7 @@ class TransportLayerClient(object):
     @log_function
     def make_query(self, destination, query_type, args, retry_on_dns_fail,
                    ignore_backoff=False):
-        path = _create_path(PREFIX, "/query/%s", query_type)
+        path = _create_v1_path("/query/%s", query_type)
 
         content = yield self.client.get_json(
             destination=destination,
@@ -231,7 +231,7 @@ class TransportLayerClient(object):
                 "make_membership_event called with membership='%s', must be one of %s" %
                 (membership, ",".join(valid_memberships))
             )
-        path = _create_path(PREFIX, "/make_%s/%s/%s", membership, room_id, user_id)
+        path = _create_v1_path("/make_%s/%s/%s", membership, room_id, user_id)
 
         ignore_backoff = False
         retry_on_dns_fail = False
@@ -258,7 +258,7 @@ class TransportLayerClient(object):
     @defer.inlineCallbacks
     @log_function
     def send_join(self, destination, room_id, event_id, content):
-        path = _create_path(PREFIX, "/send_join/%s/%s", room_id, event_id)
+        path = _create_v1_path("/send_join/%s/%s", room_id, event_id)
 
         response = yield self.client.put_json(
             destination=destination,
@@ -271,7 +271,7 @@ class TransportLayerClient(object):
     @defer.inlineCallbacks
     @log_function
     def send_leave(self, destination, room_id, event_id, content):
-        path = _create_path(PREFIX, "/send_leave/%s/%s", room_id, event_id)
+        path = _create_v1_path("/send_leave/%s/%s", room_id, event_id)
 
         response = yield self.client.put_json(
             destination=destination,
@@ -290,7 +290,7 @@ class TransportLayerClient(object):
     @defer.inlineCallbacks
     @log_function
     def send_invite(self, destination, room_id, event_id, content):
-        path = _create_path(PREFIX, "/invite/%s/%s", room_id, event_id)
+        path = _create_v1_path("/invite/%s/%s", room_id, event_id)
 
         response = yield self.client.put_json(
             destination=destination,
@@ -306,7 +306,7 @@ class TransportLayerClient(object):
     def get_public_rooms(self, remote_server, limit, since_token,
                          search_filter=None, include_all_networks=False,
                          third_party_instance_id=None):
-        path = PREFIX + "/publicRooms"
+        path = _create_v1_path("/publicRooms")
 
         args = {
             "include_all_networks": "true" if include_all_networks else "false",
@@ -332,7 +332,7 @@ class TransportLayerClient(object):
     @defer.inlineCallbacks
     @log_function
     def exchange_third_party_invite(self, destination, room_id, event_dict):
-        path = _create_path(PREFIX, "/exchange_third_party_invite/%s", room_id,)
+        path = _create_v1_path("/exchange_third_party_invite/%s", room_id,)
 
         response = yield self.client.put_json(
             destination=destination,
@@ -345,7 +345,7 @@ class TransportLayerClient(object):
     @defer.inlineCallbacks
     @log_function
     def get_event_auth(self, destination, room_id, event_id):
-        path = _create_path(PREFIX, "/event_auth/%s/%s", room_id, event_id)
+        path = _create_v1_path("/event_auth/%s/%s", room_id, event_id)
 
         content = yield self.client.get_json(
             destination=destination,
@@ -357,7 +357,7 @@ class TransportLayerClient(object):
     @defer.inlineCallbacks
     @log_function
     def send_query_auth(self, destination, room_id, event_id, content):
-        path = _create_path(PREFIX, "/query_auth/%s/%s", room_id, event_id)
+        path = _create_v1_path("/query_auth/%s/%s", room_id, event_id)
 
         content = yield self.client.post_json(
             destination=destination,
@@ -392,7 +392,7 @@ class TransportLayerClient(object):
         Returns:
             A dict containg the device keys.
         """
-        path = PREFIX + "/user/keys/query"
+        path = _create_v1_path("/user/keys/query")
 
         content = yield self.client.post_json(
             destination=destination,
@@ -419,7 +419,7 @@ class TransportLayerClient(object):
         Returns:
             A dict containg the device keys.
         """
-        path = _create_path(PREFIX, "/user/devices/%s", user_id)
+        path = _create_v1_path("/user/devices/%s", user_id)
 
         content = yield self.client.get_json(
             destination=destination,
@@ -455,7 +455,7 @@ class TransportLayerClient(object):
             A dict containg the one-time keys.
         """
 
-        path = PREFIX + "/user/keys/claim"
+        path = _create_v1_path("/user/keys/claim")
 
         content = yield self.client.post_json(
             destination=destination,
@@ -469,7 +469,7 @@ class TransportLayerClient(object):
     @log_function
     def get_missing_events(self, destination, room_id, earliest_events,
                            latest_events, limit, min_depth, timeout):
-        path = _create_path(PREFIX, "/get_missing_events/%s", room_id,)
+        path = _create_v1_path("/get_missing_events/%s", room_id,)
 
         content = yield self.client.post_json(
             destination=destination,
@@ -489,7 +489,7 @@ class TransportLayerClient(object):
     def get_group_profile(self, destination, group_id, requester_user_id):
         """Get a group profile
         """
-        path = _create_path(PREFIX, "/groups/%s/profile", group_id,)
+        path = _create_v1_path("/groups/%s/profile", group_id,)
 
         return self.client.get_json(
             destination=destination,
@@ -508,7 +508,7 @@ class TransportLayerClient(object):
             requester_user_id (str)
             content (dict): The new profile of the group
         """
-        path = _create_path(PREFIX, "/groups/%s/profile", group_id,)
+        path = _create_v1_path("/groups/%s/profile", group_id,)
 
         return self.client.post_json(
             destination=destination,
@@ -522,7 +522,7 @@ class TransportLayerClient(object):
     def get_group_summary(self, destination, group_id, requester_user_id):
         """Get a group summary
         """
-        path = _create_path(PREFIX, "/groups/%s/summary", group_id,)
+        path = _create_v1_path("/groups/%s/summary", group_id,)
 
         return self.client.get_json(
             destination=destination,
@@ -535,7 +535,7 @@ class TransportLayerClient(object):
     def get_rooms_in_group(self, destination, group_id, requester_user_id):
         """Get all rooms in a group
         """
-        path = _create_path(PREFIX, "/groups/%s/rooms", group_id,)
+        path = _create_v1_path("/groups/%s/rooms", group_id,)
 
         return self.client.get_json(
             destination=destination,
@@ -548,7 +548,7 @@ class TransportLayerClient(object):
                           content):
         """Add a room to a group
         """
-        path = _create_path(PREFIX, "/groups/%s/room/%s", group_id, room_id,)
+        path = _create_v1_path("/groups/%s/room/%s", group_id, room_id,)
 
         return self.client.post_json(
             destination=destination,
@@ -562,8 +562,8 @@ class TransportLayerClient(object):
                              config_key, content):
         """Update room in group
         """
-        path = _create_path(
-            PREFIX, "/groups/%s/room/%s/config/%s",
+        path = _create_v1_path(
+            "/groups/%s/room/%s/config/%s",
             group_id, room_id, config_key,
         )
 
@@ -578,7 +578,7 @@ class TransportLayerClient(object):
     def remove_room_from_group(self, destination, group_id, requester_user_id, room_id):
         """Remove a room from a group
         """
-        path = _create_path(PREFIX, "/groups/%s/room/%s", group_id, room_id,)
+        path = _create_v1_path("/groups/%s/room/%s", group_id, room_id,)
 
         return self.client.delete_json(
             destination=destination,
@@ -591,7 +591,7 @@ class TransportLayerClient(object):
     def get_users_in_group(self, destination, group_id, requester_user_id):
         """Get users in a group
         """
-        path = _create_path(PREFIX, "/groups/%s/users", group_id,)
+        path = _create_v1_path("/groups/%s/users", group_id,)
 
         return self.client.get_json(
             destination=destination,
@@ -604,7 +604,7 @@ class TransportLayerClient(object):
     def get_invited_users_in_group(self, destination, group_id, requester_user_id):
         """Get users that have been invited to a group
         """
-        path = _create_path(PREFIX, "/groups/%s/invited_users", group_id,)
+        path = _create_v1_path("/groups/%s/invited_users", group_id,)
 
         return self.client.get_json(
             destination=destination,
@@ -617,8 +617,8 @@ class TransportLayerClient(object):
     def accept_group_invite(self, destination, group_id, user_id, content):
         """Accept a group invite
         """
-        path = _create_path(
-            PREFIX, "/groups/%s/users/%s/accept_invite",
+        path = _create_v1_path(
+            "/groups/%s/users/%s/accept_invite",
             group_id, user_id,
         )
 
@@ -633,7 +633,7 @@ class TransportLayerClient(object):
     def join_group(self, destination, group_id, user_id, content):
         """Attempts to join a group
         """
-        path = _create_path(PREFIX, "/groups/%s/users/%s/join", group_id, user_id)
+        path = _create_v1_path("/groups/%s/users/%s/join", group_id, user_id)
 
         return self.client.post_json(
             destination=destination,
@@ -646,7 +646,7 @@ class TransportLayerClient(object):
     def invite_to_group(self, destination, group_id, user_id, requester_user_id, content):
         """Invite a user to a group
         """
-        path = _create_path(PREFIX, "/groups/%s/users/%s/invite", group_id, user_id)
+        path = _create_v1_path("/groups/%s/users/%s/invite", group_id, user_id)
 
         return self.client.post_json(
             destination=destination,
@@ -662,7 +662,7 @@ class TransportLayerClient(object):
         invited.
         """
 
-        path = _create_path(PREFIX, "/groups/local/%s/users/%s/invite", group_id, user_id)
+        path = _create_v1_path("/groups/local/%s/users/%s/invite", group_id, user_id)
 
         return self.client.post_json(
             destination=destination,
@@ -676,7 +676,7 @@ class TransportLayerClient(object):
                                user_id, content):
         """Remove a user fron a group
         """
-        path = _create_path(PREFIX, "/groups/%s/users/%s/remove", group_id, user_id)
+        path = _create_v1_path("/groups/%s/users/%s/remove", group_id, user_id)
 
         return self.client.post_json(
             destination=destination,
@@ -693,7 +693,7 @@ class TransportLayerClient(object):
         kicked from the group.
         """
 
-        path = _create_path(PREFIX, "/groups/local/%s/users/%s/remove", group_id, user_id)
+        path = _create_v1_path("/groups/local/%s/users/%s/remove", group_id, user_id)
 
         return self.client.post_json(
             destination=destination,
@@ -708,7 +708,7 @@ class TransportLayerClient(object):
         the attestations
         """
 
-        path = _create_path(PREFIX, "/groups/%s/renew_attestation/%s", group_id, user_id)
+        path = _create_v1_path("/groups/%s/renew_attestation/%s", group_id, user_id)
 
         return self.client.post_json(
             destination=destination,
@@ -723,12 +723,12 @@ class TransportLayerClient(object):
         """Update a room entry in a group summary
         """
         if category_id:
-            path = _create_path(
-                PREFIX, "/groups/%s/summary/categories/%s/rooms/%s",
+            path = _create_v1_path(
+                "/groups/%s/summary/categories/%s/rooms/%s",
                 group_id, category_id, room_id,
             )
         else:
-            path = _create_path(PREFIX, "/groups/%s/summary/rooms/%s", group_id, room_id,)
+            path = _create_v1_path("/groups/%s/summary/rooms/%s", group_id, room_id,)
 
         return self.client.post_json(
             destination=destination,
@@ -744,12 +744,12 @@ class TransportLayerClient(object):
         """Delete a room entry in a group summary
         """
         if category_id:
-            path = _create_path(
-                PREFIX + "/groups/%s/summary/categories/%s/rooms/%s",
+            path = _create_v1_path(
+                "/groups/%s/summary/categories/%s/rooms/%s",
                 group_id, category_id, room_id,
             )
         else:
-            path = _create_path(PREFIX, "/groups/%s/summary/rooms/%s", group_id, room_id,)
+            path = _create_v1_path("/groups/%s/summary/rooms/%s", group_id, room_id,)
 
         return self.client.delete_json(
             destination=destination,
@@ -762,7 +762,7 @@ class TransportLayerClient(object):
     def get_group_categories(self, destination, group_id, requester_user_id):
         """Get all categories in a group
         """
-        path = _create_path(PREFIX, "/groups/%s/categories", group_id,)
+        path = _create_v1_path("/groups/%s/categories", group_id,)
 
         return self.client.get_json(
             destination=destination,
@@ -775,7 +775,7 @@ class TransportLayerClient(object):
     def get_group_category(self, destination, group_id, requester_user_id, category_id):
         """Get category info in a group
         """
-        path = _create_path(PREFIX, "/groups/%s/categories/%s", group_id, category_id,)
+        path = _create_v1_path("/groups/%s/categories/%s", group_id, category_id,)
 
         return self.client.get_json(
             destination=destination,
@@ -789,7 +789,7 @@ class TransportLayerClient(object):
                               content):
         """Update a category in a group
         """
-        path = _create_path(PREFIX, "/groups/%s/categories/%s", group_id, category_id,)
+        path = _create_v1_path("/groups/%s/categories/%s", group_id, category_id,)
 
         return self.client.post_json(
             destination=destination,
@@ -804,7 +804,7 @@ class TransportLayerClient(object):
                               category_id):
         """Delete a category in a group
         """
-        path = _create_path(PREFIX, "/groups/%s/categories/%s", group_id, category_id,)
+        path = _create_v1_path("/groups/%s/categories/%s", group_id, category_id,)
 
         return self.client.delete_json(
             destination=destination,
@@ -817,7 +817,7 @@ class TransportLayerClient(object):
     def get_group_roles(self, destination, group_id, requester_user_id):
         """Get all roles in a group
         """
-        path = _create_path(PREFIX, "/groups/%s/roles", group_id,)
+        path = _create_v1_path("/groups/%s/roles", group_id,)
 
         return self.client.get_json(
             destination=destination,
@@ -830,7 +830,7 @@ class TransportLayerClient(object):
     def get_group_role(self, destination, group_id, requester_user_id, role_id):
         """Get a roles info
         """
-        path = _create_path(PREFIX, "/groups/%s/roles/%s", group_id, role_id,)
+        path = _create_v1_path("/groups/%s/roles/%s", group_id, role_id,)
 
         return self.client.get_json(
             destination=destination,
@@ -844,7 +844,7 @@ class TransportLayerClient(object):
                           content):
         """Update a role in a group
         """
-        path = _create_path(PREFIX, "/groups/%s/roles/%s", group_id, role_id,)
+        path = _create_v1_path("/groups/%s/roles/%s", group_id, role_id,)
 
         return self.client.post_json(
             destination=destination,
@@ -858,7 +858,7 @@ class TransportLayerClient(object):
     def delete_group_role(self, destination, group_id, requester_user_id, role_id):
         """Delete a role in a group
         """
-        path = _create_path(PREFIX, "/groups/%s/roles/%s", group_id, role_id,)
+        path = _create_v1_path("/groups/%s/roles/%s", group_id, role_id,)
 
         return self.client.delete_json(
             destination=destination,
@@ -873,12 +873,12 @@ class TransportLayerClient(object):
         """Update a users entry in a group
         """
         if role_id:
-            path = _create_path(
-                PREFIX, "/groups/%s/summary/roles/%s/users/%s",
+            path = _create_v1_path(
+                "/groups/%s/summary/roles/%s/users/%s",
                 group_id, role_id, user_id,
             )
         else:
-            path = _create_path(PREFIX, "/groups/%s/summary/users/%s", group_id, user_id,)
+            path = _create_v1_path("/groups/%s/summary/users/%s", group_id, user_id,)
 
         return self.client.post_json(
             destination=destination,
@@ -893,7 +893,7 @@ class TransportLayerClient(object):
                               content):
         """Sets the join policy for a group
         """
-        path = _create_path(PREFIX, "/groups/%s/settings/m.join_policy", group_id,)
+        path = _create_v1_path("/groups/%s/settings/m.join_policy", group_id,)
 
         return self.client.put_json(
             destination=destination,
@@ -909,12 +909,12 @@ class TransportLayerClient(object):
         """Delete a users entry in a group
         """
         if role_id:
-            path = _create_path(
-                PREFIX, "/groups/%s/summary/roles/%s/users/%s",
+            path = _create_v1_path(
+                "/groups/%s/summary/roles/%s/users/%s",
                 group_id, role_id, user_id,
             )
         else:
-            path = _create_path(PREFIX, "/groups/%s/summary/users/%s", group_id, user_id,)
+            path = _create_v1_path("/groups/%s/summary/users/%s", group_id, user_id,)
 
         return self.client.delete_json(
             destination=destination,
@@ -927,7 +927,7 @@ class TransportLayerClient(object):
         """Get the groups a list of users are publicising
         """
 
-        path = PREFIX + "/get_groups_publicised"
+        path = _create_v1_path("/get_groups_publicised")
 
         content = {"user_ids": user_ids}
 
@@ -939,20 +939,22 @@ class TransportLayerClient(object):
         )
 
 
-def _create_path(prefix, path, *args):
-    """Creates a path from the prefix, path template and args. Ensures that
-    all args are url encoded.
+def _create_v1_path(path, *args):
+    """Creates a path against V1 federation API from the path template and
+    args. Ensures that all args are url encoded.
 
     Example:
 
-        _create_path(PREFIX, "/event/%s/", event_id)
+        _create_v1_path("/event/%s/", event_id)
 
     Args:
-        prefix (str)
         path (str): String template for the path
         args: ([str]): Args to insert into path. Each arg will be url encoded
 
     Returns:
         str
     """
-    return prefix + path % tuple(urllib.parse.quote(arg, "") for arg in args)
+    return (
+        FEDERATION_V1_PREFIX
+        + path % tuple(urllib.parse.quote(arg, "") for arg in args)
+    )
diff --git a/synapse/federation/transport/server.py b/synapse/federation/transport/server.py
index 3553f418f..e592269cf 100644
--- a/synapse/federation/transport/server.py
+++ b/synapse/federation/transport/server.py
@@ -22,7 +22,7 @@ from twisted.internet import defer
 
 import synapse
 from synapse.api.errors import Codes, FederationDeniedError, SynapseError
-from synapse.api.urls import FEDERATION_PREFIX as PREFIX
+from synapse.api.urls import FEDERATION_V1_PREFIX
 from synapse.http.endpoint import parse_and_validate_server_name
 from synapse.http.server import JsonResource
 from synapse.http.servlet import (
@@ -227,6 +227,8 @@ class BaseFederationServlet(object):
     """
     REQUIRE_AUTH = True
 
+    PREFIX = FEDERATION_V1_PREFIX  # Allows specifying the API version
+
     def __init__(self, handler, authenticator, ratelimiter, server_name):
         self.handler = handler
         self.authenticator = authenticator
@@ -286,7 +288,7 @@ class BaseFederationServlet(object):
         return new_func
 
     def register(self, server):
-        pattern = re.compile("^" + PREFIX + self.PATH + "$")
+        pattern = re.compile("^" + self.PREFIX + self.PATH + "$")
 
         for method in ("GET", "PUT", "POST"):
             code = getattr(self, "on_%s" % (method), None)