diff --git a/synapse/handlers/device.py b/synapse/handlers/device.py
index 52e9af17d9dc..aba393bc5586 100644
--- a/synapse/handlers/device.py
+++ b/synapse/handlers/device.py
@@ -1212,9 +1212,18 @@ async def multi_user_device_resync(
             raise InvalidAPICallError(f"Only one origin permitted, got {origins!r}")
 
         result = {}
+        failed = set()
         # TODO(Perf): Actually batch these up
         for user_id in user_ids:
-            result[user_id] = await self.user_device_resync(user_id)
+            user_result, user_failed = await self._user_device_resync_returning_failed(
+                user_id
+            )
+            result[user_id] = user_result
+            if user_failed:
+                failed.add(user_id)
+
+        if mark_failed_as_stale:
+            await self.store.mark_remote_users_device_caches_as_stale(failed)
 
         return result
 
@@ -1226,7 +1235,7 @@ async def user_device_resync(
         if failed and mark_failed_as_stale:
             # Mark the remote user's device list as stale so we know we need to retry
             # it later.
-            await self.store.mark_remote_user_device_cache_as_stale(user_id)
+            await self.store.mark_remote_users_device_caches_as_stale((user_id,))
 
         return result
 
diff --git a/synapse/handlers/devicemessage.py b/synapse/handlers/devicemessage.py
index 444c08bc2eef..8cc21529b443 100644
--- a/synapse/handlers/devicemessage.py
+++ b/synapse/handlers/devicemessage.py
@@ -195,7 +195,7 @@ async def _check_for_unknown_devices(
                 sender_user_id,
                 unknown_devices,
             )
-            await self.store.mark_remote_user_device_cache_as_stale(sender_user_id)
+            await self.store.mark_remote_users_device_caches_as_stale((sender_user_id,))
 
             # Immediately attempt a resync in the background
             run_in_background(self._user_device_resync, user_id=sender_user_id)
diff --git a/synapse/handlers/federation_event.py b/synapse/handlers/federation_event.py
index f7223b03c364..00e815d765d9 100644
--- a/synapse/handlers/federation_event.py
+++ b/synapse/handlers/federation_event.py
@@ -1420,7 +1420,7 @@ async def _resync_device(self, sender: str) -> None:
         """
 
         try:
-            await self._store.mark_remote_user_device_cache_as_stale(sender)
+            await self._store.mark_remote_users_device_caches_as_stale((sender,))
 
             # Immediately attempt a resync in the background
             if self._config.worker.worker_app:
diff --git a/synapse/storage/databases/main/devices.py b/synapse/storage/databases/main/devices.py
index 534f7fc04a54..7e93bb56bdac 100644
--- a/synapse/storage/databases/main/devices.py
+++ b/synapse/storage/databases/main/devices.py
@@ -54,7 +54,7 @@
     AbstractStreamIdTracker,
     StreamIdGenerator,
 )
-from synapse.types import JsonDict, get_verify_key_from_cross_signing_key
+from synapse.types import JsonDict, StrCollection, get_verify_key_from_cross_signing_key
 from synapse.util import json_decoder, json_encoder
 from synapse.util.caches.descriptors import cached, cachedList
 from synapse.util.caches.lrucache import LruCache
@@ -1026,16 +1026,30 @@ async def get_user_ids_requiring_device_list_resync(
 
         return {row["user_id"] for row in rows}
 
-    async def mark_remote_user_device_cache_as_stale(self, user_id: str) -> None:
+    async def mark_remote_users_device_caches_as_stale(
+        self, user_ids: StrCollection
+    ) -> None:
         """Records that the server has reason to believe the cache of the devices
         for the remote users is out of date.
         """
-        await self.db_pool.simple_upsert(
-            table="device_lists_remote_resync",
-            keyvalues={"user_id": user_id},
-            values={},
-            insertion_values={"added_ts": self._clock.time_msec()},
-            desc="mark_remote_user_device_cache_as_stale",
+
+        def _mark_remote_users_device_caches_as_stale_txn(
+            txn: LoggingTransaction,
+        ) -> None:
+            # TODO add insertion_values support to simple_upsert_many and use
+            #      that!
+            for user_id in user_ids:
+                self.db_pool.simple_upsert_txn(
+                    txn,
+                    table="device_lists_remote_resync",
+                    keyvalues={"user_id": user_id},
+                    values={},
+                    insertion_values={"added_ts": self._clock.time_msec()},
+                )
+
+        await self.db_pool.runInteraction(
+            "mark_remote_users_device_caches_as_stale",
+            _mark_remote_users_device_caches_as_stale_txn,
         )
 
     async def mark_remote_user_device_cache_as_valid(self, user_id: str) -> None:
diff --git a/synapse/types.py b/synapse/types.py
index f2d436ddc38c..0c725eb9677d 100644
--- a/synapse/types.py
+++ b/synapse/types.py
@@ -77,6 +77,10 @@
 # A JSON-serialisable object.
 JsonSerializable = object
 
+# Collection[str] that does not include str itself; str being a Sequence[str]
+# is very misleading and results in bugs.
+StrCollection = Union[Tuple[str, ...], List[str], Set[str]]
+
 
 # Note that this seems to require inheriting *directly* from Interface in order
 # for mypy-zope to realize it is an interface.