diff --git a/sanic/app.py b/sanic/app.py
index 65a6196f..63e466ec 100644
--- a/sanic/app.py
+++ b/sanic/app.py
@@ -1,7 +1,7 @@
 import logging
 import re
 import warnings
-from asyncio import get_event_loop
+from asyncio import get_event_loop, ensure_future, CancelledError
 from collections import deque, defaultdict
 from functools import partial
 from inspect import isawaitable, stack, getmodulename
@@ -54,6 +54,7 @@ class Sanic:
         self.listeners = defaultdict(list)
         self.is_running = False
         self.websocket_enabled = False
+        self.websocket_tasks = []
 
         # Register alternative method names
         self.go_fast = self.run
@@ -178,7 +179,7 @@ class Sanic:
         :param host:
         :return: decorated function
         """
-        self.websocket_enabled = True
+        self.enable_websocket()
 
         # Fix case where the user did not prefix the URL with a /
         # and will probably get confused as to why it's not working
@@ -190,11 +191,17 @@ class Sanic:
                 request.app = self
                 protocol = request.transport.get_protocol()
                 ws = await protocol.websocket_handshake(request)
+
+                # schedule the application handler
+                # its future is kept in self.websocket_tasks in case it
+                # needs to be cancelled due to the server being stopped
+                fut = ensure_future(handler(request, ws, *args, **kwargs))
+                self.websocket_tasks.append(fut)
                 try:
-                    # invoke the application handler
-                    await handler(request, ws, *args, **kwargs)
-                except ConnectionClosed:
+                    await fut
+                except (CancelledError, ConnectionClosed):
                     pass
+                self.websocket_tasks.remove(fut)
                 await ws.close()
 
             self.router.add(uri=uri, handler=websocket_handler,
@@ -213,6 +220,14 @@ class Sanic:
         Websocket is enabled automatically if websocket routes are
         added to the application.
         """
+        if not self.websocket_enabled:
+            # if the server is stopped, we want to cancel any ongoing
+            # websocket tasks, to allow the server to exit promptly
+            @self.listener('before_server_stop')
+            def cancel_websocket_tasks(app, loop):
+                for task in self.websocket_tasks:
+                    task.cancel()
+
         self.websocket_enabled = enable
 
     def remove_route(self, uri, clean_cache=True, host=None):