diff --git a/changelog.d/6968.bugfix b/changelog.d/6968.bugfix
new file mode 100644
index 000000000..9965bfc0c
--- /dev/null
+++ b/changelog.d/6968.bugfix
@@ -0,0 +1 @@
+Fix `duplicate key` error which was logged when rejoining a room over federation.
diff --git a/synapse/handlers/federation.py b/synapse/handlers/federation.py
index a689065f8..fb0a586ea 100644
--- a/synapse/handlers/federation.py
+++ b/synapse/handlers/federation.py
@@ -1323,16 +1323,18 @@ class FederationHandler(BaseHandler):
 
             logger.debug("do_invite_join event: %s", event)
 
-            try:
-                await self.store.store_room(
-                    room_id=room_id,
-                    room_creator_user_id="",
-                    is_public=False,
-                    room_version=room_version_obj,
-                )
-            except Exception:
-                # FIXME
-                pass
+            # if this is the first time we've joined this room, it's time to add
+            # a row to `rooms` with the correct room version. If there's already a
+            # row there, we should override it, since it may have been populated
+            # based on an invite request which lied about the room version.
+            #
+            # federation_client.send_join has already checked that the room
+            # version in the received create event is the same as room_version_obj,
+            # so we can rely on it now.
+            #
+            await self.store.upsert_room_on_join(
+                room_id=room_id, room_version=room_version_obj,
+            )
 
             await self._persist_auth_tree(
                 origin, auth_chain, state, event, room_version_obj
diff --git a/synapse/storage/data_stores/main/room.py b/synapse/storage/data_stores/main/room.py
index 9a17e336b..70137dfbe 100644
--- a/synapse/storage/data_stores/main/room.py
+++ b/synapse/storage/data_stores/main/room.py
@@ -954,6 +954,23 @@ class RoomStore(RoomBackgroundUpdateStore, RoomWorkerStore, SearchStore):
 
         self.config = hs.config
 
+    async def upsert_room_on_join(self, room_id: str, room_version: RoomVersion):
+        """Ensure that the room is stored in the table
+
+        Called when we join a room over federation, and overwrites any room version
+        currently in the table.
+        """
+        await self.db.simple_upsert(
+            desc="upsert_room_on_join",
+            table="rooms",
+            keyvalues={"room_id": room_id},
+            values={"room_version": room_version.identifier},
+            insertion_values={"is_public": False, "creator": ""},
+            # rooms has a unique constraint on room_id, so no need to lock when doing an
+            # emulated upsert.
+            lock=False,
+        )
+
     @defer.inlineCallbacks
     def store_room(
         self,