diff --git a/tools/run-dev b/tools/run-dev
index 0f4e4112f8..d6231ded6c 100755
--- a/tools/run-dev
+++ b/tools/run-dev
@@ -92,10 +92,17 @@ if options.test:
     settings_module = "zproject.test_settings"
     # Don't auto-reload when running Puppeteer tests
     runserver_args = ["--noreload"]
-    tornado_autoreload = []
+    runtornado_command = ["./manage.py", "runtornado"]
 else:
     settings_module = "zproject.settings"
-    tornado_autoreload = ["-m", "tornado.autoreload"]
+    runtornado_command = [
+        "-m",
+        "tornado.autoreload",
+        "--until-success",
+        "./manage.py",
+        "runtornado",
+        "--autoreload",
+    ]
 
 manage_args = [f"--settings={settings_module}"]
 os.environ["DJANGO_SETTINGS_MODULE"] = settings_module
@@ -148,9 +155,7 @@ def server_processes() -> List[List[str]]:
             "env",
             "PYTHONUNBUFFERED=1",
             "python3",
-            *tornado_autoreload,
-            "./manage.py",
-            "runtornado",
+            *runtornado_command,
             *manage_args,
             f"127.0.0.1:{tornado_port}",
         ],
diff --git a/zerver/management/commands/runtornado.py b/zerver/management/commands/runtornado.py
index 707e99bf00..af76c05eb1 100644
--- a/zerver/management/commands/runtornado.py
+++ b/zerver/management/commands/runtornado.py
@@ -8,12 +8,9 @@ from urllib.parse import SplitResult
 from asgiref.sync import async_to_sync, sync_to_async
 from django.conf import settings
 from django.core.management.base import BaseCommand, CommandError, CommandParser
-from tornado import autoreload
 from tornado.platform.asyncio import AsyncIOMainLoop
 from typing_extensions import override
 
-import __main__
-
 settings.RUNNING_INSIDE_TORNADO = True
 if settings.PRODUCTION:
     settings.SECURE_PROXY_SSL_HEADER = ("HTTP_X_FORWARDED_PROTO", "https")
@@ -42,6 +39,7 @@ class Command(BaseCommand):
 
     @override
     def add_arguments(self, parser: CommandParser) -> None:
+        parser.add_argument("--autoreload", action="store_true", help="Enable Tornado autoreload")
         parser.add_argument(
             "addrport",
             help="[port number or ipaddr:port]",
@@ -118,7 +116,7 @@ class Command(BaseCommand):
                     )
 
                 # Application is an instance of Django's standard wsgi handler.
-                application = create_tornado_application()
+                application = create_tornado_application(autoreload=options["autoreload"])
 
                 # start tornado web server in single-threaded mode
                 http_server = httpserver.HTTPServer(application, xheaders=True)
@@ -135,14 +133,6 @@ class Command(BaseCommand):
                 if settings.USING_RABBITMQ:
                     setup_tornado_rabbitmq(queue_client)
 
-                if hasattr(__main__, "add_reload_hook"):
-                    autoreload.start()
-
                 await stop_fut
 
-                # Monkey patch tornado.autoreload to prevent it from continuing
-                # to watch for changes after catching our SystemExit. Otherwise
-                # the user needs to press Ctrl+C twice.
-                __main__.wait = lambda: None
-
         async_to_sync(inner_run, force_new_loop=True)()
diff --git a/zerver/tornado/application.py b/zerver/tornado/application.py
index fc8b0c12b6..9215ed99d2 100644
--- a/zerver/tornado/application.py
+++ b/zerver/tornado/application.py
@@ -12,7 +12,7 @@ def setup_tornado_rabbitmq(queue_client: TornadoQueueClient) -> None:  # nocover
     autoreload.add_reload_hook(lambda: queue_client.close())
 
 
-def create_tornado_application() -> tornado.web.Application:
+def create_tornado_application(*, autoreload: bool = False) -> tornado.web.Application:
     django_handler = BaseHandler()
     django_handler.load_middleware()
 
@@ -26,7 +26,7 @@ def create_tornado_application() -> tornado.web.Application:
     return tornado.web.Application(
         [(url, AsyncDjangoHandler, dict(django_handler=django_handler)) for url in urls],
         debug=settings.DEBUG,
-        autoreload=False,
+        autoreload=autoreload,
         # Disable Tornado's own request logging, since we have our own
         log_function=lambda x: None,
     )