diff --git a/synapse/handlers/sliding_sync.py b/synapse/handlers/sliding_sync.py
index 778dddb400..7a734f6712 100644
--- a/synapse/handlers/sliding_sync.py
+++ b/synapse/handlers/sliding_sync.py
@@ -494,8 +494,7 @@ async def current_sync_for_user(
 
         # Assemble sliding window lists
         lists: Dict[str, SlidingSyncResult.SlidingWindowList] = {}
-        # Keep track of the rooms that we're going to display and need to fetch more
-        # info about
+        # Keep track of the rooms that we can display and need to fetch more info about
         relevant_room_map: Dict[str, RoomSyncConfig] = {}
         if has_lists and sync_config.lists is not None:
             sync_room_map = await self.filter_rooms_relevant_for_sync(
@@ -623,6 +622,8 @@ async def current_sync_for_user(
 
         # Filter out rooms that haven't received updates and we've sent down
         # previously.
+        # Keep track of the rooms that we're going to display and need to fetch more info about
+        relevant_rooms_to_send_map = relevant_room_map
         if from_token:
             rooms_should_send = set()
 
@@ -660,7 +661,7 @@ async def current_sync_for_user(
                 relevant_room_map.keys(), from_token.stream_token.room_key
             )
             rooms_should_send.update(rooms_that_have_updates)
-            relevant_room_map = {
+            relevant_rooms_to_send_map = {
                 room_id: room_sync_config
                 for room_id, room_sync_config in relevant_room_map.items()
                 if room_id in rooms_should_send
@@ -672,7 +673,7 @@ async def handle_room(room_id: str) -> None:
             room_sync_result = await self.get_room_sync_data(
                 sync_config=sync_config,
                 room_id=room_id,
-                room_sync_config=relevant_room_map[room_id],
+                room_sync_config=relevant_rooms_to_send_map[room_id],
                 room_membership_for_user_at_to_token=room_membership_for_user_map[
                     room_id
                 ],
@@ -684,17 +685,19 @@ async def handle_room(room_id: str) -> None:
             if room_sync_result or not from_token:
                 rooms[room_id] = room_sync_result
 
-        if relevant_room_map:
+        if relevant_rooms_to_send_map:
             with start_active_span("sliding_sync.generate_room_entries"):
-                await concurrently_execute(handle_room, relevant_room_map, 10)
+                await concurrently_execute(handle_room, relevant_rooms_to_send_map, 10)
 
         extensions = await self.get_extensions_response(
             sync_config=sync_config,
             actual_lists=lists,
-            # TODO: Once https://github.com/element-hq/synapse/pull/17479 merges, this
-            # will need to be updated to make sure it includes everything before the
-            # pre-filter on `relevant_room_map`.
-            actual_room_ids=set(rooms.keys()),
+            # We're purposely using `relevant_room_map` instead of
+            # `relevant_rooms_to_send_map` here. This needs to be all room_ids we could
+            # send regardless of whether they have an event update or not. The
+            # extensions care about more than just normal events in the rooms (like
+            # account data, read receipts, typing indicators, to-device messages, etc).
+            actual_room_ids=set(relevant_room_map.keys()),
             actual_room_response_map=rooms,
             from_token=from_token,
             to_token=to_token,
@@ -704,7 +707,7 @@ async def handle_room(room_id: str) -> None:
             connection_position = await self.connection_store.record_rooms(
                 sync_config=sync_config,
                 from_token=from_token,
-                sent_room_ids=relevant_room_map.keys(),
+                sent_room_ids=relevant_rooms_to_send_map.keys(),
                 # TODO: We need to calculate which rooms have had updates since the `from_token` but were not included in the `sent_room_ids`
                 unsent_room_ids=[],
             )
diff --git a/tests/rest/client/test_sync.py b/tests/rest/client/test_sync.py
index 9c3426b02c..1184adde70 100644
--- a/tests/rest/client/test_sync.py
+++ b/tests/rest/client/test_sync.py
@@ -6657,15 +6657,7 @@ def test_receipts_incremental_sync(self) -> None:
             exact=True,
         )
         # No events in the timeline since they were sent before the `from_token`
-        self.assertIncludes(
-            {
-                event["event_id"]
-                for event in response_body["rooms"][room_id1].get("timeline", [])
-            },
-            set(),
-            exact=True,
-            message=str(response_body["rooms"][room_id1]),
-        )
+        self.assertNotIn(room_id1, response_body["rooms"])
 
         # Check room3:
         #
@@ -6694,15 +6686,7 @@ def test_receipts_incremental_sync(self) -> None:
             exact=True,
         )
         # No events in the timeline since they were sent before the `from_token`
-        self.assertIncludes(
-            {
-                event["event_id"]
-                for event in response_body["rooms"][room_id3].get("timeline", [])
-            },
-            set(),
-            exact=True,
-            message=str(response_body["rooms"][room_id3]),
-        )
+        self.assertNotIn(room_id3, response_body["rooms"])
 
     def test_receipts_incremental_sync_all_live_receipts(self) -> None:
         """