diff --git a/api_docs/changelog.md b/api_docs/changelog.md
index 8007bbac64..fea33cafa9 100644
--- a/api_docs/changelog.md
+++ b/api_docs/changelog.md
@@ -20,6 +20,29 @@ format used by the Zulip server that they are interacting with.
 
 ## Changes in Zulip 9.0
 
+**Feature level 263**:
+
+* `POST /users/me/presence`: A new `last_update_id`
+  parameter can be given, instructing
+  the server to only fetch presence data with `last_update_id`
+  greater than the value provided. The server also provides
+  a `presence_last_update_id` field in the response, which
+  tells the client the greatest `last_update_id` of the fetched
+  presence data. This can then be used as the value in the
+  aforementioned parameter to avoid re-fetching of already known
+  data when polling the endpoint next time.
+  Additionally, the client specifying the `last_update_id`
+  implies it uses the modern API format, so
+  `slim_presence=true` will be assumed by the server.
+
+
+* [`POST /register`](/api/register-queue): The response now also
+  includes a `presence_last_update_id` field, with the same
+  meaning as described above for `/users/me/presence`.
+  In the same way, the retrieved value can be passed when
+  querying `/users/me/presence` to avoid re-fetching of already
+  known data.
+
 **Feature level 262**:
 
 * [`GET /users/{user_id}/status`](/api/get-user-status): Added a new
diff --git a/version.py b/version.py
index 1a3f1b56a2..a2ead205cb 100644
--- a/version.py
+++ b/version.py
@@ -33,7 +33,7 @@ DESKTOP_WARNING_VERSION = "5.9.3"
 # Changes should be accompanied by documentation explaining what the
 # new level means in api_docs/changelog.md, as well as "**Changes**"
 # entries in the endpoint's documentation in `zulip.yaml`.
-API_FEATURE_LEVEL = 262
+API_FEATURE_LEVEL = 263
 
 # Bump the minor PROVISION_VERSION to indicate that folks should provision
 # only when going from an old version of the code to a newer version. Bump
diff --git a/zerver/lib/events.py b/zerver/lib/events.py
index b33368e2f2..983ac42456 100644
--- a/zerver/lib/events.py
+++ b/zerver/lib/events.py
@@ -123,6 +123,7 @@ def fetch_initial_state_data(
     user_avatar_url_field_optional: bool = False,
     user_settings_object: bool = False,
     slim_presence: bool = False,
+    presence_last_update_id_fetched_by_client: Optional[int] = None,
     include_subscribers: bool = True,
     include_streams: bool = True,
     spectator_requested_language: Optional[str] = None,
@@ -229,11 +230,23 @@ def fetch_initial_state_data(
         state["muted_users"] = [] if user_profile is None else get_user_mutes(user_profile)
 
     if want("presence"):
-        state["presences"] = (
-            {}
-            if user_profile is None
-            else get_presences_for_realm(realm, slim_presence, user_profile)
-        )
+        if presence_last_update_id_fetched_by_client is not None:
+            # This param being submitted by the client, means they want to use
+            # the modern API.
+            slim_presence = True
+
+        if user_profile is not None:
+            presences, presence_last_update_id_fetched_by_server = get_presences_for_realm(
+                realm,
+                slim_presence,
+                last_update_id_fetched_by_client=presence_last_update_id_fetched_by_client,
+                requesting_user_profile=user_profile,
+            )
+            state["presences"] = presences
+            state["presence_last_update_id"] = presence_last_update_id_fetched_by_server
+        else:
+            state["presences"] = {}
+
         # Send server_timestamp, to match the format of `GET /presence` requests.
         state["server_timestamp"] = time.time()
 
@@ -1304,6 +1317,15 @@ def apply_event(
         else:
             raise AssertionError("Unexpected event type {type}/{op}".format(**event))
     elif event["type"] == "presence":
+        # Note: Fetch_initial_state_data includes
+        # a presence_last_update_id value, reflecting the Max .last_update_id
+        # value of the UserPresence objects in the data. Events don't carry
+        # information about the last_update_id of the UserPresence object
+        # to which they correspond, so we don't (and can't) attempt to update that initial
+        # presence data here.
+        # This means that the state resulting from fetch_initial_state + apply_events will not
+        # match the state of a hypothetical fetch_initial_state fetch that included the fully
+        # updated data. This is intended and not a bug.
         if slim_presence:
             user_key = str(event["user_id"])
         else:
@@ -1559,6 +1581,7 @@ def do_events_register(
     apply_markdown: bool = True,
     client_gravatar: bool = False,
     slim_presence: bool = False,
+    presence_last_update_id_fetched_by_client: Optional[int] = None,
     event_types: Optional[Sequence[str]] = None,
     queue_lifespan_secs: int = 0,
     all_public_streams: bool = False,
@@ -1608,8 +1631,9 @@ def do_events_register(
             user_avatar_url_field_optional=user_avatar_url_field_optional,
             user_settings_object=user_settings_object,
             user_list_incomplete=user_list_incomplete,
-            # slim_presence is a noop, because presence is not included.
+            # These presence params are a noop, because presence is not included.
             slim_presence=True,
+            presence_last_update_id_fetched_by_client=None,
             # Force include_subscribers=False for security reasons.
             include_subscribers=include_subscribers,
             # Force include_streams=False for security reasons.
@@ -1656,6 +1680,7 @@ def do_events_register(
         user_avatar_url_field_optional=user_avatar_url_field_optional,
         user_settings_object=user_settings_object,
         slim_presence=slim_presence,
+        presence_last_update_id_fetched_by_client=presence_last_update_id_fetched_by_client,
         include_subscribers=include_subscribers,
         include_streams=include_streams,
         pronouns_field_type_supported=pronouns_field_type_supported,
diff --git a/zerver/lib/home.py b/zerver/lib/home.py
index 028d0fe3e4..4981d77a26 100644
--- a/zerver/lib/home.py
+++ b/zerver/lib/home.py
@@ -169,6 +169,7 @@ def build_page_params_for_home_page_load(
             apply_markdown=True,
             client_gravatar=True,
             slim_presence=True,
+            presence_last_update_id_fetched_by_client=-1,
             client_capabilities=client_capabilities,
             narrow=narrow,
             include_streams=False,
diff --git a/zerver/lib/presence.py b/zerver/lib/presence.py
index 9cd9fa2d5f..00b19beda5 100644
--- a/zerver/lib/presence.py
+++ b/zerver/lib/presence.py
@@ -1,7 +1,7 @@
 import time
 from collections import defaultdict
 from datetime import datetime, timedelta
-from typing import Any, Dict, Mapping, Optional, Sequence
+from typing import Any, Dict, Mapping, Optional, Sequence, Tuple
 
 from django.conf import settings
 from django.utils.timezone import now as timezone_now
@@ -147,14 +147,25 @@ def get_presence_for_user(
 
 
 def get_presence_dict_by_realm(
-    realm: Realm, slim_presence: bool = False, requesting_user_profile: Optional[UserProfile] = None
-) -> Dict[str, Dict[str, Any]]:
+    realm: Realm,
+    slim_presence: bool = False,
+    last_update_id_fetched_by_client: Optional[int] = None,
+    requesting_user_profile: Optional[UserProfile] = None,
+) -> Tuple[Dict[str, Dict[str, Any]], int]:
     two_weeks_ago = timezone_now() - timedelta(weeks=2)
+    kwargs: Dict[str, object] = dict()
+    if last_update_id_fetched_by_client is not None:
+        kwargs["last_update_id__gt"] = last_update_id_fetched_by_client
+
     query = UserPresence.objects.filter(
         realm_id=realm.id,
-        last_connected_time__gte=two_weeks_ago,
         user_profile__is_active=True,
         user_profile__is_bot=False,
+        # We can consider tweaking this value when last_update_id is being used,
+        # to potentially fetch more data since such a client is expected to only
+        # do it once and then only do small, incremental fetches.
+        last_connected_time__gte=two_weeks_ago,
+        **kwargs,
     )
 
     if settings.CAN_ACCESS_ALL_USERS_GROUP_LIMITS_PRESENCE and not check_user_can_access_all_users(
@@ -172,26 +183,67 @@ def get_presence_dict_by_realm(
             "user_profile_id",
             "user_profile__enable_offline_push_notifications",
             "user_profile__date_joined",
+            "last_update_id",
         )
     )
+    # Get max last_update_id from the list.
+    if presence_rows:
+        last_update_id_fetched_by_server: Optional[int] = max(
+            row["last_update_id"] for row in presence_rows
+        )
+    elif last_update_id_fetched_by_client is not None:
+        # If there are no results, that means that are no new updates to presence
+        # since what the client has last seen. Therefore, returning the same
+        # last_update_id that the client provided is correct.
+        last_update_id_fetched_by_server = last_update_id_fetched_by_client
+    else:
+        # If the client didn't specify a last_update_id, we return -1 to indicate
+        # the lack of any data fetched, while sticking to the convention of
+        # returning an integer.
+        last_update_id_fetched_by_server = -1
 
-    return get_presence_dicts_for_rows(presence_rows, slim_presence)
+    assert last_update_id_fetched_by_server is not None
+    return get_presence_dicts_for_rows(
+        presence_rows, slim_presence
+    ), last_update_id_fetched_by_server
 
 
 def get_presences_for_realm(
-    realm: Realm, slim_presence: bool, requesting_user_profile: UserProfile
-) -> Dict[str, Dict[str, Dict[str, Any]]]:
+    realm: Realm,
+    slim_presence: bool,
+    last_update_id_fetched_by_client: Optional[int],
+    requesting_user_profile: UserProfile,
+) -> Tuple[Dict[str, Dict[str, Dict[str, Any]]], Optional[int]]:
     if realm.presence_disabled:
         # Return an empty dict if presence is disabled in this realm
-        return defaultdict(dict)
+        return defaultdict(dict), None
 
-    return get_presence_dict_by_realm(realm, slim_presence, requesting_user_profile)
+    return get_presence_dict_by_realm(
+        realm,
+        slim_presence,
+        last_update_id_fetched_by_client,
+        requesting_user_profile=requesting_user_profile,
+    )
 
 
 def get_presence_response(
-    requesting_user_profile: UserProfile, slim_presence: bool
+    requesting_user_profile: UserProfile,
+    slim_presence: bool,
+    last_update_id_fetched_by_client: Optional[int] = None,
 ) -> Dict[str, Any]:
     realm = requesting_user_profile.realm
     server_timestamp = time.time()
-    presences = get_presences_for_realm(realm, slim_presence, requesting_user_profile)
-    return dict(presences=presences, server_timestamp=server_timestamp)
+    presences, last_update_id_fetched_by_server = get_presences_for_realm(
+        realm,
+        slim_presence,
+        last_update_id_fetched_by_client,
+        requesting_user_profile=requesting_user_profile,
+    )
+
+    response_dict = dict(
+        presences=presences,
+        server_timestamp=server_timestamp,
+        presence_last_update_id=last_update_id_fetched_by_server,
+    )
+
+    return response_dict
diff --git a/zerver/models/presence.py b/zerver/models/presence.py
index e4adbc5222..a83daf83ed 100644
--- a/zerver/models/presence.py
+++ b/zerver/models/presence.py
@@ -30,6 +30,13 @@ class UserPresence(models.Model):
     # queries to fetch all presence data for a given realm.
     realm = models.ForeignKey(Realm, on_delete=CASCADE)
 
+    # The sequence ID within this realm for the last update to this user's presence;
+    # these IDs are generated by the PresenceSequence table and an important part
+    # of how we send incremental presence updates efficiently.
+    # To put it simply, every time we update a UserPresence row in a realm,
+    # the row gets last_update_id equal to 1 more than the previously updated
+    # row in that realm.
+    # This allows us to order UserPresence rows by when they were last updated.
     last_update_id = models.PositiveBigIntegerField(db_index=True, default=0)
 
     # The last time the user had a client connected to Zulip,
@@ -77,6 +84,17 @@ class UserPresence(models.Model):
 
 
 class PresenceSequence(models.Model):
+    """
+    This table is used to generate last_update_id values in the UserPresence table.
+
+    It serves as a per-realm sequence generator, while also facilitating
+    locking to avoid concurrency issues with setting last_update_id values.
+
+    Every realm has its unique row in this table, and when a UserPresence in the realm
+    is being updated, this row get locked against other UserPresence updates in the realm
+    to ensure sequential processing and set last_update_id values correctly.
+    """
+
     realm = models.OneToOneField(Realm, on_delete=CASCADE)
     last_update_id = models.PositiveBigIntegerField()
 
diff --git a/zerver/openapi/zulip.yaml b/zerver/openapi/zulip.yaml
index 9a49c0886f..6f6e3844f6 100644
--- a/zerver/openapi/zulip.yaml
+++ b/zerver/openapi/zulip.yaml
@@ -13156,6 +13156,20 @@ paths:
                             either the user's ID or the user's Zulip API email.
                           additionalProperties:
                             $ref: "#/components/schemas/Presence"
+                      presence_last_update_id:
+                        type: integer
+                        description: |
+                          Present if `presence` is present in `fetch_event_types`.
+
+                          Provides the `last_update_id` value of the latest presence data fetched by
+                          the server and included in the response in `presences`. This can be used
+                          as the value of the `presence_last_update_id` parameter when polling
+                          for presence data at the /users/me/presence endpoint to tell the server
+                          to only fetch the relevant newer data in order to skip redundant
+                          already-known presence information.
+
+                          **Changes**: New in Zulip 9.0 (feature level 263).
+
                       server_timestamp:
                         type: number
                         description: |
diff --git a/zerver/tests/test_events.py b/zerver/tests/test_events.py
index 7cfc78123a..d017c4979d 100644
--- a/zerver/tests/test_events.py
+++ b/zerver/tests/test_events.py
@@ -425,6 +425,11 @@ class BaseAction(ZulipTestCase):
                 state["realm_bots"] = {u["email"]: u for u in state["realm_bots"]}
             # Since time is different for every call, just fix the value
             state["server_timestamp"] = 0
+            if "presence_last_update_id" in state:
+                # We don't adjust presence_last_update_id via apply_events,
+                # since events don't carry the relevant information.
+                # Fix the value just like server_timestamp.
+                state["presence_last_update_id"] = 0
 
         normalize(state1)
         normalize(state2)
diff --git a/zerver/tests/test_home.py b/zerver/tests/test_home.py
index c4e575cb82..fd2edef9b9 100644
--- a/zerver/tests/test_home.py
+++ b/zerver/tests/test_home.py
@@ -114,6 +114,7 @@ class HomeTest(ZulipTestCase):
         "password_min_guesses",
         "password_min_length",
         "presences",
+        "presence_last_update_id",
         "queue_id",
         "realm_add_custom_emoji_policy",
         "realm_allow_edit_history",
diff --git a/zerver/tests/test_presence.py b/zerver/tests/test_presence.py
index 84a63328f2..39dbba21c4 100644
--- a/zerver/tests/test_presence.py
+++ b/zerver/tests/test_presence.py
@@ -37,23 +37,28 @@ class UserPresenceModelTests(ZulipTestCase):
 
         user_profile = self.example_user("hamlet")
         email = user_profile.email
-        presence_dct = get_presence_dict_by_realm(user_profile.realm)
+        presence_dct, last_update_id = get_presence_dict_by_realm(user_profile.realm)
         self.assert_length(presence_dct, 0)
+        self.assertEqual(last_update_id, -1)
 
         self.login_user(user_profile)
         result = self.client_post("/json/users/me/presence", {"status": "active"})
         self.assert_json_success(result)
 
+        actual_last_update_id = UserPresence.objects.all().latest("last_update_id").last_update_id
+
         slim_presence = False
-        presence_dct = get_presence_dict_by_realm(user_profile.realm, slim_presence)
+        presence_dct, last_update_id = get_presence_dict_by_realm(user_profile.realm, slim_presence)
         self.assert_length(presence_dct, 1)
         self.assertEqual(presence_dct[email]["website"]["status"], "active")
+        self.assertEqual(last_update_id, actual_last_update_id)
 
         slim_presence = True
-        presence_dct = get_presence_dict_by_realm(user_profile.realm, slim_presence)
+        presence_dct, last_update_id = get_presence_dict_by_realm(user_profile.realm, slim_presence)
         self.assert_length(presence_dct, 1)
         info = presence_dct[str(user_profile.id)]
         self.assertEqual(set(info.keys()), {"active_timestamp", "idle_timestamp"})
+        self.assertEqual(last_update_id, actual_last_update_id)
 
         def back_date(num_weeks: int) -> None:
             user_presence = UserPresence.objects.get(user_profile=user_profile)
@@ -64,20 +69,73 @@ class UserPresenceModelTests(ZulipTestCase):
 
         # Simulate the presence being a week old first.  Nothing should change.
         back_date(num_weeks=1)
-        presence_dct = get_presence_dict_by_realm(user_profile.realm)
+        presence_dct, last_update_id = get_presence_dict_by_realm(user_profile.realm)
         self.assert_length(presence_dct, 1)
+        self.assertEqual(last_update_id, actual_last_update_id)
 
         # If the UserPresence row is three weeks old, we ignore it.
         back_date(num_weeks=3)
-        presence_dct = get_presence_dict_by_realm(user_profile.realm)
+        presence_dct, last_update_id = get_presence_dict_by_realm(user_profile.realm)
         self.assert_length(presence_dct, 0)
+        self.assertEqual(last_update_id, -1)
 
         # If the values are set to "never", ignore it just like for sufficiently old presence rows.
         UserPresence.objects.filter(id=user_profile.id).update(
             last_active_time=None, last_connected_time=None
         )
-        presence_dct = get_presence_dict_by_realm(user_profile.realm)
+        presence_dct, last_update_id = get_presence_dict_by_realm(user_profile.realm)
         self.assert_length(presence_dct, 0)
+        self.assertEqual(last_update_id, -1)
+
+    def test_last_update_id_logic(self) -> None:
+        slim_presence = True
+        UserPresence.objects.all().delete()
+
+        user_profile = self.example_user("hamlet")
+        presence_dct, last_update_id = get_presence_dict_by_realm(
+            user_profile.realm, slim_presence, last_update_id_fetched_by_client=-1
+        )
+        self.assert_length(presence_dct, 0)
+        self.assertEqual(last_update_id, -1)
+
+        self.login_user(user_profile)
+        result = self.client_post("/json/users/me/presence", {"status": "active"})
+        self.assert_json_success(result)
+
+        actual_last_update_id = UserPresence.objects.all().latest("last_update_id").last_update_id
+
+        presence_dct, last_update_id = get_presence_dict_by_realm(
+            user_profile.realm, slim_presence, last_update_id_fetched_by_client=-1
+        )
+        self.assert_length(presence_dct, 1)
+        self.assertEqual(last_update_id, actual_last_update_id)
+
+        # Now pass last_update_id as of this latest fetch. The server should only query for data
+        # updated after that. There's no such data, so we get no presence data back and the
+        # returned last_update_id remains the same.
+        presence_dct, last_update_id = get_presence_dict_by_realm(
+            user_profile.realm,
+            slim_presence,
+            last_update_id_fetched_by_client=actual_last_update_id,
+        )
+        self.assert_length(presence_dct, 0)
+        self.assertEqual(last_update_id, actual_last_update_id)
+
+        # Now generate a new update in the realm.
+        iago = self.example_user("iago")
+        self.login_user(iago)
+        result = self.client_post("/json/users/me/presence", {"status": "active"})
+
+        # There's a new update now, so we can expect it to be fetched; and no older data.
+        presence_dct, last_update_id = get_presence_dict_by_realm(
+            user_profile.realm,
+            slim_presence,
+            last_update_id_fetched_by_client=actual_last_update_id,
+        )
+        self.assert_length(presence_dct, 1)
+        self.assertEqual(presence_dct.keys(), {str(iago.id)})
+        # last_update_id is incremented due to the new update.
+        self.assertEqual(last_update_id, actual_last_update_id + 1)
 
     def test_pushable_always_false(self) -> None:
         # This field was never used by clients of the legacy API, so we
@@ -92,7 +150,7 @@ class UserPresenceModelTests(ZulipTestCase):
         self.assert_json_success(result)
 
         def pushable() -> bool:
-            presence_dct = get_presence_dict_by_realm(user_profile.realm)
+            presence_dct, _ = get_presence_dict_by_realm(user_profile.realm)
             self.assert_length(presence_dct, 1)
             return presence_dct[email]["website"]["pushable"]
 
@@ -139,6 +197,108 @@ class UserPresenceTests(ZulipTestCase):
         result = self.client_post("/json/users/me/presence", {"status": "foo"})
         self.assert_json_error(result, "Invalid status: foo")
 
+    def test_last_update_id_api(self) -> None:
+        UserPresence.objects.all().delete()
+
+        hamlet = self.example_user("hamlet")
+        othello = self.example_user("othello")
+
+        self.login_user(hamlet)
+
+        params = dict(status="idle", last_update_id=-1)
+        result = self.client_post("/json/users/me/presence", params)
+        json = self.assert_json_success(result)
+        self.assertEqual(set(json["presences"].keys()), {str(hamlet.id)})
+
+        # In tests, the presence update is processed immediately rather than in the background
+        # in the queue worker, so we see it reflected immediately.
+        # In production, our presence update may be processed with some delay, so the last_update_id
+        # might not include it yet. In such a case, we'd see the original value of -1 returned,
+        # due to there being no new data to return.
+        last_update_id = UserPresence.objects.latest("last_update_id").last_update_id
+        self.assertEqual(json["presence_last_update_id"], last_update_id)
+
+        # Briefly test that we include presence_last_update_id in the response
+        # also in the legacy format API with slim_presence=False.
+        # Re-doing an idle status so soon doesn't cause updates
+        # so this doesn't mutate any state.
+        params = dict(status="idle", slim_presence="false")
+        result = self.client_post("/json/users/me/presence", params)
+        json = self.assert_json_success(result)
+        self.assertEqual(json["presence_last_update_id"], last_update_id)
+
+        self.login_user(othello)
+        params = dict(status="idle", last_update_id=-1)
+        result = self.client_post("/json/users/me/presence", params)
+        json = self.assert_json_success(result)
+        self.assertEqual(set(json["presences"].keys()), {str(hamlet.id), str(othello.id)})
+        self.assertEqual(json["presence_last_update_id"], last_update_id + 1)
+
+        last_update_id += 1
+        # Immediately sending an idle status again doesn't cause updates, so the server
+        # doesn't have any new data since last_update_id to return.
+        params = dict(status="idle", last_update_id=last_update_id)
+        result = self.client_post("/json/users/me/presence", params)
+        json = self.assert_json_success(result)
+        self.assertEqual(set(json["presences"].keys()), set())
+        # No new data, so the last_update_id is returned back.
+        self.assertEqual(json["presence_last_update_id"], last_update_id)
+
+        # hamlet sends an active status. othello will next check presence and we'll
+        # want to verify he gets hamlet's update and nothing else.
+        self.login_user(hamlet)
+        params = dict(status="active", last_update_id=-1)
+        result = self.client_post("/json/users/me/presence", params)
+        json = self.assert_json_success(result)
+
+        # Make sure UserPresence.last_update_id is incremented.
+        self.assertEqual(
+            UserPresence.objects.latest("last_update_id").last_update_id, last_update_id + 1
+        )
+
+        # Now othello checks presence and should get hamlet's update.
+        self.login_user(othello)
+        params = dict(status="idle", last_update_id=last_update_id)
+        result = self.client_post("/json/users/me/presence", params)
+        json = self.assert_json_success(result)
+        self.assertEqual(set(json["presences"].keys()), {str(hamlet.id)})
+        self.assertEqual(json["presence_last_update_id"], last_update_id + 1)
+
+    def test_last_update_id_api_no_data_edge_cases(self) -> None:
+        hamlet = self.example_user("hamlet")
+
+        self.login_user(hamlet)
+
+        UserPresence.objects.all().delete()
+
+        params = dict(status="idle", last_update_id=-1)
+        # Make do_update_user_presence a noop. This simulates a production-like environment
+        # where the update is processed in a queue worker, so hamlet may not see his update
+        # reflected back to him in the response. Therefore it is as if there is no presence
+        # data.
+        # In such a situation, he should get his last_update_id=-1 back.
+        with mock.patch("zerver.worker.user_presence.do_update_user_presence"):
+            result = self.client_post("/json/users/me/presence", params)
+        json = self.assert_json_success(result)
+
+        self.assertEqual(set(json["presences"].keys()), set())
+        self.assertEqual(json["presence_last_update_id"], -1)
+        self.assertFalse(UserPresence.objects.exists())
+
+        # Now check the same, but hamlet doesn't pass last_update_id at all,
+        # like an old slim_presence client would due to an implementation
+        # prior to the introduction of last_update_id.
+        params = dict(status="idle")
+        with mock.patch("zerver.worker.user_presence.do_update_user_presence"):
+            result = self.client_post("/json/users/me/presence", params)
+        json = self.assert_json_success(result)
+        self.assertEqual(set(json["presences"].keys()), set())
+
+        # When there's no data and the client didn't provide a last_update_id
+        # value that we could reflect back to it, we fall back to -1.
+        self.assertEqual(json["presence_last_update_id"], -1)
+        self.assertFalse(UserPresence.objects.exists())
+
     def test_set_idle(self) -> None:
         client = "website"
 
diff --git a/zerver/views/events_register.py b/zerver/views/events_register.py
index 520b340d39..8b793a7e57 100644
--- a/zerver/views/events_register.py
+++ b/zerver/views/events_register.py
@@ -145,6 +145,7 @@ def events_register_backend(
         apply_markdown,
         client_gravatar,
         slim_presence,
+        None,
         event_types,
         queue_lifespan_secs,
         all_public_streams,
diff --git a/zerver/views/presence.py b/zerver/views/presence.py
index 67a5f330a3..b25cd3c6f3 100644
--- a/zerver/views/presence.py
+++ b/zerver/views/presence.py
@@ -154,7 +154,13 @@ def update_active_status_backend(
     ping_only: Json[bool] = False,
     new_user_input: Json[bool] = False,
     slim_presence: Json[bool] = False,
+    last_update_id: Optional[Json[int]] = None,
 ) -> HttpResponse:
+    if last_update_id is not None:
+        # This param being submitted by the client, means they want to use
+        # the modern API.
+        slim_presence = True
+
     status_val = UserPresence.status_from_string(status)
     if status_val is None:
         raise JsonableError(_("Invalid status: {status}").format(status=status))
@@ -166,7 +172,9 @@ def update_active_status_backend(
     if ping_only:
         ret: Dict[str, Any] = {}
     else:
-        ret = get_presence_response(user_profile, slim_presence)
+        ret = get_presence_response(
+            user_profile, slim_presence, last_update_id_fetched_by_client=last_update_id
+        )
 
     if user_profile.realm.is_zephyr_mirror_realm:
         # In zephyr mirroring realms, users can't see the presence of other
@@ -190,4 +198,8 @@ def get_statuses_for_realm(request: HttpRequest, user_profile: UserProfile) -> H
     # This isn't used by the web app; it's available for API use by
     # bots and other clients.  We may want to add slim_presence
     # support for it (or just migrate its API wholesale) later.
-    return json_success(request, data=get_presence_response(user_profile, slim_presence=False))
+    data = get_presence_response(user_profile, slim_presence=False)
+
+    # We're not interested in the last_update_id field in this context.
+    data.pop("presence_last_update_id", None)
+    return json_success(request, data=data)