diff --git a/awx/main/wsrelay.py b/awx/main/wsrelay.py
index c3ab95836e..09d7dfe92b 100644
--- a/awx/main/wsrelay.py
+++ b/awx/main/wsrelay.py
@@ -245,13 +245,13 @@ class WebSocketRelayManager(object):
                 if action == "online":
                     self.known_hosts[hostname] = ip
                 elif action == "offline":
-                    self.cleanup_offline_host(hostname)
+                    await self.cleanup_offline_host(hostname)
             except Exception as e:
                 # This catch-all is the same as the one above. asyncio will eat the exception
                 # but we want to know about it.
                 logger.exception(f"on_ws_heartbeat exception: {e}")
 
-    def cleanup_offline_host(self, hostname):
+    async def cleanup_offline_host(self, hostname):
         """
         Given a hostname, try to cancel its task/connection and remove it from
         the list of hosts we know about.
@@ -260,6 +260,19 @@ class WebSocketRelayManager(object):
         """
         if hostname in self.relay_connections:
             self.relay_connections[hostname].cancel()
+
+            # Wait for the task to actually run its cancel/completion logic
+            # otherwise it might get GC'd too early when we del it below.
+            # Being GC'd too early could generate a scary message in logs:
+            # "Task was destroyed but it is pending!"
+            try:
+                await asyncio.wait_for(self.relay_connections[hostname].async_task, timeout=10)
+            except asyncio.TimeoutError:
+                logger.warning(f"Tried to cancel relay connection for {hostname} but it timed out during cleanup.")
+            except asyncio.CancelledError:
+                # Handle the case where the task was already cancelled by the time we got here.
+                pass
+
             del self.relay_connections[hostname]
 
         if hostname in self.known_hosts:
@@ -314,13 +327,11 @@ class WebSocketRelayManager(object):
 
             if deleted_remote_hosts:
                 logger.info(f"Removing {deleted_remote_hosts} from websocket broadcast list")
+                await asyncio.gather(self.cleanup_offline_host(h) for h in deleted_remote_hosts)
 
             if new_remote_hosts:
                 logger.info(f"Adding {new_remote_hosts} to websocket broadcast list")
 
-            for h in deleted_remote_hosts:
-                self.cleanup_offline_host(h)
-
             for h in new_remote_hosts:
                 stats = self.stats_mgr.new_remote_host_stats(h)
                 relay_connection = WebsocketRelayConnection(name=self.local_hostname, stats=stats, remote_host=self.known_hosts[h])