diff --git a/zerver/tests/test_event_system.py b/zerver/tests/test_event_system.py
index 924a524662..93f60a3b10 100644
--- a/zerver/tests/test_event_system.py
+++ b/zerver/tests/test_event_system.py
@@ -36,6 +36,7 @@ from zerver.tornado.event_queue import (
     allocate_client_descriptor,
     clear_client_event_queues_for_testing,
     get_client_info_for_message_event,
+    mark_clients_to_reload,
     process_message_event,
     send_web_reload_client_events,
 )
@@ -1141,7 +1142,10 @@ class WebReloadClientsTest(ZulipTestCase):
         client = allocate_client_descriptor(queue_data)
 
         send_web_reload_client_events()
+        self.assert_length(client.event_queue.queue, 0)
 
+        mark_clients_to_reload([client.event_queue.id])
+        send_web_reload_client_events()
         self.assert_length(client.event_queue.queue, 1)
         reload_event = client.event_queue.queue[0]
 
diff --git a/zerver/tests/test_events.py b/zerver/tests/test_events.py
index 533fec669e..44f433819d 100644
--- a/zerver/tests/test_events.py
+++ b/zerver/tests/test_events.py
@@ -251,6 +251,7 @@ from zerver.tornado.event_queue import (
     allocate_client_descriptor,
     clear_client_event_queues_for_testing,
     create_heartbeat_event,
+    mark_clients_to_reload,
     send_web_reload_client_events,
 )
 from zerver.views.realm_playgrounds import access_playground_by_id
@@ -288,6 +289,7 @@ class BaseAction(ZulipTestCase):
         pronouns_field_type_supported: bool = True,
         linkifier_url_template: bool = True,
         user_list_incomplete: bool = False,
+        client_is_old: bool = False,
     ) -> List[Dict[str, Any]]:
         """
         Make sure we have a clean slate of client descriptors for these tests.
@@ -336,6 +338,9 @@ class BaseAction(ZulipTestCase):
             user_list_incomplete=user_list_incomplete,
         )
 
+        if client_is_old:
+            mark_clients_to_reload([client.event_queue.id])
+
         # We want even those `send_event` calls which have been hooked to
         # `transaction.on_commit` to execute in tests.
         # See the comment in `ZulipTestCase.capture_send_event_calls`.
@@ -3457,8 +3462,14 @@ class NormalActionsTest(BaseAction):
         check_has_zoom_token("events[0]", events[0], value=False)
 
     def test_web_reload_client_event(self) -> None:
+        self.verify_action(
+            lambda: send_web_reload_client_events(),
+            client_is_old=False,
+            num_events=0,
+            state_change_expected=False,
+        )
         with self.assertRaises(WebReloadClientError):
-            self.verify_action(lambda: send_web_reload_client_events())
+            self.verify_action(lambda: send_web_reload_client_events(), client_is_old=True)
 
     def test_display_setting_event_not_sent(self) -> None:
         events = self.verify_action(
diff --git a/zerver/tornado/event_queue.py b/zerver/tornado/event_queue.py
index e7c9d38fdf..647dba7009 100644
--- a/zerver/tornado/event_queue.py
+++ b/zerver/tornado/event_queue.py
@@ -19,6 +19,7 @@ from typing import (
     Dict,
     Iterable,
     List,
+    Literal,
     Mapping,
     MutableMapping,
     Optional,
@@ -443,6 +444,11 @@ def prune_internal_data(events: List[Dict[str, Any]]) -> List[Dict[str, Any]]:
     return events
 
 
+# Queue-ids which still need to be sent a web_reload_client event.
+# This is treated as an ordered set, which is sorted by realm-id when
+# loaded from disk.
+web_reload_clients: Dict[str, Literal[True]] = {}
+
 # maps queue ids to client descriptors
 clients: Dict[str, ClientDescriptor] = {}
 # maps user id to list of client descriptors
@@ -461,6 +467,7 @@ gc_hooks: List[Callable[[int, ClientDescriptor, bool], None]] = []
 def clear_client_event_queues_for_testing() -> None:
     assert settings.TEST_SUITE
     clients.clear()
+    web_reload_clients.clear()
     user_clients.clear()
     realm_clients_all_streams.clear()
     gc_hooks.clear()
@@ -530,6 +537,8 @@ def do_gc_event_queues(
         filter_client_dict(realm_clients_all_streams, realm_id)
 
     for id in to_remove:
+        if id in web_reload_clients:
+            del web_reload_clients[id]
         for cb in gc_hooks:
             cb(
                 clients[id].user_profile_id,
@@ -615,6 +624,8 @@ def load_event_queues(port: int) -> None:
                 "Tornado %d could not deserialize event queues", port, stack_info=True
             )
 
+    mark_clients_to_reload(clients.keys())
+
     for client in clients.values():
         # Put code for migrations due to event queue data format changes here
 
@@ -642,12 +653,30 @@ def send_restart_events() -> None:
             client.add_event(event)
 
 
-def send_web_reload_client_events(immediate: bool = False) -> None:
+def mark_clients_to_reload(queue_ids: Iterable[str]) -> None:
+    # Build web_reload_clients, which is a sorted-by-realm-id list of
+    # website client queue-ids which were were loaded from old Tornado
+    # instances.  We use an (ordered) dict to make removing one be
+    # O(1), as well as pulling an ordered N of them to be O(N).  We
+    # sort by realm_id so that restarts are rolling by realm.
+    for qid in sorted(
+        (qid for qid in queue_ids if clients[qid].accepts_event({"type": "web_reload_client"})),
+        key=lambda qid: clients[qid].realm_id,
+    ):
+        web_reload_clients[qid] = True
+
+
+def send_web_reload_client_events(immediate: bool = False, count: Optional[int] = None) -> None:
     event: Dict[str, Any] = dict(
         type="web_reload_client",
         immediate=immediate,
     )
-    for client in clients.values():
+    if count is None:
+        count = len(web_reload_clients)
+    queue_ids = list(web_reload_clients.keys())[:count]
+    for qid in queue_ids:
+        del web_reload_clients[qid]
+        client = clients[qid]
         if client.accepts_event(event):
             client.add_event(event)