diff --git a/changelog.d/12683.bugfix b/changelog.d/12683.bugfix
new file mode 100644
index 000000000..2ce84a223
--- /dev/null
+++ b/changelog.d/12683.bugfix
@@ -0,0 +1 @@
+Fix a bug introduced in Synapse 1.57.0 where `/messages` would throw a 500 error when querying for a non-existent room.
diff --git a/synapse/handlers/pagination.py b/synapse/handlers/pagination.py
index 7ee334037..2e3018009 100644
--- a/synapse/handlers/pagination.py
+++ b/synapse/handlers/pagination.py
@@ -448,7 +448,7 @@ class PaginationHandler:
             )
             # We expect `/messages` to use historic pagination tokens by default but
             # `/messages` should still works with live tokens when manually provided.
-            assert from_token.room_key.topological
+            assert from_token.room_key.topological is not None
 
         if pagin_config.limit is None:
             # This shouldn't happen as we've set a default limit before this
diff --git a/synapse/storage/databases/main/stream.py b/synapse/storage/databases/main/stream.py
index 793e90663..4e1d9647b 100644
--- a/synapse/storage/databases/main/stream.py
+++ b/synapse/storage/databases/main/stream.py
@@ -785,22 +785,14 @@ class StreamWorkerStore(EventsWorkerStore, SQLBaseStore):
         return None
 
     async def get_current_room_stream_token_for_room_id(
-        self, room_id: Optional[str] = None
+        self, room_id: str
     ) -> RoomStreamToken:
-        """Returns the current position of the rooms stream.
-
-        By default, it returns a live token with the current global stream
-        token. Specifying a `room_id` causes it to return a historic token with
-        the room specific topological token.
-        """
+        """Returns the current position of the rooms stream (historic token)."""
         stream_ordering = self.get_room_max_stream_ordering()
-        if room_id is None:
-            return RoomStreamToken(None, stream_ordering)
-        else:
-            topo = await self.db_pool.runInteraction(
-                "_get_max_topological_txn", self._get_max_topological_txn, room_id
-            )
-            return RoomStreamToken(topo, stream_ordering)
+        topo = await self.db_pool.runInteraction(
+            "_get_max_topological_txn", self._get_max_topological_txn, room_id
+        )
+        return RoomStreamToken(topo, stream_ordering)
 
     def get_stream_id_for_event_txn(
         self,
@@ -870,7 +862,11 @@ class StreamWorkerStore(EventsWorkerStore, SQLBaseStore):
         )
 
         rows = txn.fetchall()
-        return rows[0][0] if rows else 0
+        # An aggregate function like MAX() will always return one row per group
+        # so we can safely rely on the lookup here. For example, when a we
+        # lookup a `room_id` which does not exist, `rows` will look like
+        # `[(None,)]`
+        return rows[0][0] if rows[0][0] is not None else 0
 
     @staticmethod
     def _set_before_and_after(