diff --git a/python/ray/serve/_private/long_poll.py b/python/ray/serve/_private/long_poll.py
index 6d0ea42a16dd..f3538913b76b 100644
--- a/python/ray/serve/_private/long_poll.py
+++ b/python/ray/serve/_private/long_poll.py
@@ -88,7 +88,11 @@ def __init__(
         self.key_listeners = key_listeners
         self.event_loop = call_in_event_loop
         self.snapshot_ids: Dict[KeyType, int] = {
-            key: -1 for key in self.key_listeners.keys()
+            # The initial snapshot id for each key is < 0,
+            # but real snapshot keys in the long poll host are always >= 0,
+            # so this will always trigger an initial update.
+            key: -1
+            for key in self.key_listeners.keys()
         }
         self.is_running = True
 
@@ -191,11 +195,9 @@ def __init__(
         ] = LISTEN_FOR_CHANGE_REQUEST_TIMEOUT_S,
     ):
         # Map object_key -> int
-        self.snapshot_ids: DefaultDict[KeyType, int] = defaultdict(
-            lambda: random.randint(0, 1_000_000)
-        )
+        self.snapshot_ids: Dict[KeyType, int] = {}
         # Map object_key -> object
-        self.object_snapshots: Dict[KeyType, Any] = dict()
+        self.object_snapshots: Dict[KeyType, Any] = {}
         # Map object_key -> set(asyncio.Event waiting for updates)
         self.notifier_events: DefaultDict[KeyType, Set[asyncio.Event]] = defaultdict(
             set
@@ -247,16 +249,24 @@ async def listen_for_change(
         immediately if the snapshot_ids are outdated, otherwise it will block
         until there's an update.
         """
-        watched_keys = keys_to_snapshot_ids.keys()
-        existent_keys = set(watched_keys).intersection(set(self.snapshot_ids.keys()))
-
         # If there are any keys with outdated snapshot ids,
         # return their updated values immediately.
-        updated_objects = {
-            key: UpdatedObject(self.object_snapshots[key], self.snapshot_ids[key])
-            for key in existent_keys
-            if self.snapshot_ids[key] != keys_to_snapshot_ids[key]
-        }
+        updated_objects = {}
+        for key, client_snapshot_id in keys_to_snapshot_ids.items():
+            try:
+                existing_id = self.snapshot_ids[key]
+            except KeyError:
+                # The caller may ask for keys that we don't know about (yet),
+                # just ignore them.
+                # This can happen when, for example,
+                # a deployment handle is manually created for an app
+                # that hasn't been deployed yet (by bypassing the safety checks).
+                continue
+
+            if existing_id != client_snapshot_id:
+                updated_objects[key] = UpdatedObject(
+                    self.object_snapshots[key], existing_id
+                )
         if len(updated_objects) > 0:
             self._count_send(updated_objects)
             return updated_objects
@@ -264,7 +274,7 @@ async def listen_for_change(
         # Otherwise, register asyncio events to be waited.
         async_task_to_events = {}
         async_task_to_watched_keys = {}
-        for key in watched_keys:
+        for key in keys_to_snapshot_ids.keys():
             # Create a new asyncio event for this key.
             event = asyncio.Event()
 
@@ -398,10 +408,16 @@ def notify_changed(
         object_key: KeyType,
         updated_object: Any,
     ):
-        self.snapshot_ids[object_key] += 1
+        try:
+            self.snapshot_ids[object_key] += 1
+        except KeyError:
+            # Initial snapshot id must be >= 0, so that the long poll client
+            # can send a negative initial snapshot id to get a fast update.
+            # They should also be randomized;
+            # see https://github.com/ray-project/ray/pull/45881#discussion_r1645243485
+            self.snapshot_ids[object_key] = random.randint(0, 1_000_000)
         self.object_snapshots[object_key] = updated_object
         logger.debug(f"LongPollHost: Notify change for key {object_key}.")
 
-        if object_key in self.notifier_events:
-            for event in self.notifier_events.pop(object_key):
-                event.set()
+        for event in self.notifier_events.pop(object_key, set()):
+            event.set()