diff --git a/changelog.d/9516.bugfix b/changelog.d/9516.bugfix
new file mode 100644
index 000000000000..81188c5473eb
--- /dev/null
+++ b/changelog.d/9516.bugfix
@@ -0,0 +1 @@
+Fix a bug where users' pushers were not all deleted when they deactivated their account.
diff --git a/scripts/synapse_port_db b/scripts/synapse_port_db
index d2aaea08f55c..58edf6af6c8c 100755
--- a/scripts/synapse_port_db
+++ b/scripts/synapse_port_db
@@ -47,6 +47,7 @@ from synapse.storage.databases.main.events_bg_updates import (
 from synapse.storage.databases.main.media_repository import (
     MediaRepositoryBackgroundUpdateStore,
 )
+from synapse.storage.databases.main.pusher import PusherWorkerStore
 from synapse.storage.databases.main.registration import (
     RegistrationBackgroundUpdateStore,
     find_max_generated_user_id_localpart,
@@ -177,6 +178,7 @@ class Store(
     UserDirectoryBackgroundUpdateStore,
     EndToEndKeyBackgroundStore,
     StatsStore,
+    PusherWorkerStore,
 ):
     def execute(self, f, *args, **kwargs):
         return self.db_pool.runInteraction(f.__name__, f, *args, **kwargs)
diff --git a/synapse/storage/databases/main/pusher.py b/synapse/storage/databases/main/pusher.py
index 74219cb05ead..6b608ebc9bb1 100644
--- a/synapse/storage/databases/main/pusher.py
+++ b/synapse/storage/databases/main/pusher.py
@@ -39,6 +39,11 @@ def __init__(self, database: DatabasePool, db_conn: Connection, hs: "HomeServer"
             db_conn, "pushers", "id", extra_tables=[("deleted_pushers", "stream_id")]
         )
 
+        self.db_pool.updates.register_background_update_handler(
+            "remove_deactivated_pushers",
+            self._remove_deactivated_pushers,
+        )
+
     def _decode_pushers_rows(self, rows: Iterable[dict]) -> Iterator[PusherConfig]:
         """JSON-decode the data in the rows returned from the `pushers` table
 
@@ -284,6 +289,54 @@ async def set_throttle_params(
             lock=False,
         )
 
+    async def _remove_deactivated_pushers(self, progress: dict, batch_size: int) -> int:
+        """A background update that deletes all pushers for deactivated users.
+
+        Note that we don't proacively tell the pusherpool that we've deleted
+        these (just because its a bit off a faff to do from here), but they will
+        get cleaned up at the next restart
+        """
+
+        last_user = progress.get("last_user", "")
+
+        def _delete_pushers(txn) -> int:
+
+            sql = """
+                SELECT name FROM users
+                WHERE deactivated = ? and name > ?
+                ORDER BY name ASC
+                LIMIT ?
+            """
+
+            txn.execute(sql, (1, last_user, batch_size))
+            users = [row[0] for row in txn]
+
+            self.db_pool.simple_delete_many_txn(
+                txn,
+                table="pushers",
+                column="user_name",
+                iterable=users,
+                keyvalues={},
+            )
+
+            if users:
+                self.db_pool.updates._background_update_progress_txn(
+                    txn, "remove_deactivated_pushers", {"last_user": users[-1]}
+                )
+
+            return len(users)
+
+        number_deleted = await self.db_pool.runInteraction(
+            "_remove_deactivated_pushers", _delete_pushers
+        )
+
+        if number_deleted < batch_size:
+            await self.db_pool.updates._end_background_update(
+                "remove_deactivated_pushers"
+            )
+
+        return number_deleted
+
 
 class PusherStore(PusherWorkerStore):
     def get_pushers_stream_token(self) -> int:
diff --git a/synapse/storage/databases/main/schema/delta/59/08delete_pushers_for_deactivated_accounts.sql b/synapse/storage/databases/main/schema/delta/59/08delete_pushers_for_deactivated_accounts.sql
index 20ba4abca30f..0ec6764150ec 100644
--- a/synapse/storage/databases/main/schema/delta/59/08delete_pushers_for_deactivated_accounts.sql
+++ b/synapse/storage/databases/main/schema/delta/59/08delete_pushers_for_deactivated_accounts.sql
@@ -14,8 +14,7 @@
  */
 
 
--- We may not have deleted all pushers for deactivated accounts. Do so now.
---
--- Note: We don't bother updating the `deleted_pushers` table as it's just use
--- to stop pushers on workers, and that will happen when they get next restarted.
-DELETE FROM pushers WHERE user_name IN (SELECT name FROM users WHERE deactivated = 1);
+-- We may not have deleted all pushers for deactivated accounts, so we set up a
+-- background job to delete them.
+INSERT INTO background_updates (ordering, update_name, progress_json) VALUES
+  (5908, 'remove_deactivated_pushers', '{}');