diff --git a/changelog.d/15314.feature b/changelog.d/15314.feature
index 68b289b0cc7c..5ce0c029cee2 100644
--- a/changelog.d/15314.feature
+++ b/changelog.d/15314.feature
@@ -1 +1 @@
-Experimental support for passing One Time Key requests to application services ([MSC3983](https://github.com/matrix-org/matrix-spec-proposals/pull/3983)).
+Experimental support for passing One Time Key and device key requests to application services ([MSC3983](https://github.com/matrix-org/matrix-spec-proposals/pull/3983) and [MSC3984](https://github.com/matrix-org/matrix-spec-proposals/pull/3984)).
diff --git a/changelog.d/15321.feature b/changelog.d/15321.feature
new file mode 100644
index 000000000000..5ce0c029cee2
--- /dev/null
+++ b/changelog.d/15321.feature
@@ -0,0 +1 @@
+Experimental support for passing One Time Key and device key requests to application services ([MSC3983](https://github.com/matrix-org/matrix-spec-proposals/pull/3983) and [MSC3984](https://github.com/matrix-org/matrix-spec-proposals/pull/3984)).
diff --git a/synapse/appservice/api.py b/synapse/appservice/api.py
index 51ee0e79df10..4685179d031e 100644
--- a/synapse/appservice/api.py
+++ b/synapse/appservice/api.py
@@ -444,6 +444,44 @@ async def claim_client_keys(
 
         return response, missing
 
+    async def query_keys(
+        self, service: "ApplicationService", query: Dict[str, List[str]]
+    ) -> Dict[str, Dict[str, Dict[str, JsonDict]]]:
+        """Query the application service for keys.
+
+        Args:
+            query: An iterable of tuples of (user ID, device ID, algorithm).
+
+        Returns:
+            A map of device_keys/master_keys/self_signing_keys/user_signing_keys:
+
+            device_keys is a map of user ID -> a map device ID -> device info.
+        """
+        if service.url is None:
+            return {}
+
+        # This is required by the configuration.
+        assert service.hs_token is not None
+
+        uri = f"{service.url}/_matrix/app/unstable/org.matrix.msc3984/keys/query"
+        try:
+            response = await self.post_json_get_json(
+                uri,
+                query,
+                headers={"Authorization": [f"Bearer {service.hs_token}"]},
+            )
+        except CodeMessageException as e:
+            # The appservice doesn't support this endpoint.
+            if e.code == 404 or e.code == 405:
+                return {}
+            logger.warning("claim_keys to %s received %s", uri, e.code)
+            return {}
+        except Exception as ex:
+            logger.warning("claim_keys to %s threw exception %s", uri, ex)
+            return {}
+
+        return response
+
     def _serialize(
         self, service: "ApplicationService", events: Iterable[EventBase]
     ) -> List[JsonDict]:
diff --git a/synapse/config/experimental.py b/synapse/config/experimental.py
index 53e6fc2b54d6..7687c80ea080 100644
--- a/synapse/config/experimental.py
+++ b/synapse/config/experimental.py
@@ -79,6 +79,11 @@ def read_config(self, config: JsonDict, **kwargs: Any) -> None:
             "msc3983_appservice_otk_claims", False
         )
 
+        # MSC3984: Proxying key queries to exclusive ASes.
+        self.msc3984_appservice_key_query: bool = experimental.get(
+            "msc3984_appservice_key_query", False
+        )
+
         # MSC3706 (server-side support for partial state in /send_join responses)
         # Synapse will always serve partial state responses to requests using the stable
         # query parameter `omit_members`. If this flag is set, Synapse will also serve
diff --git a/synapse/handlers/appservice.py b/synapse/handlers/appservice.py
index 953df4d9cd26..089dec1ad94f 100644
--- a/synapse/handlers/appservice.py
+++ b/synapse/handlers/appservice.py
@@ -18,6 +18,7 @@
     Dict,
     Iterable,
     List,
+    Mapping,
     Optional,
     Tuple,
     Union,
@@ -901,3 +902,56 @@ async def claim_e2e_one_time_keys(
                 missing.extend(result[1])
 
         return claimed_keys, missing
+
+    async def query_keys(
+        self, query: Mapping[str, Optional[List[str]]]
+    ) -> Dict[str, Dict[str, Dict[str, JsonDict]]]:
+        """Query application services for device keys.
+
+        Args:
+            query: map from user_id to a list of devices to query
+
+        Returns:
+            A map from user_id -> device_id -> device details
+        """
+        services = self.store.get_app_services()
+
+        # Partition the users by appservice.
+        query_by_appservice: Dict[str, Dict[str, List[str]]] = {}
+        for user_id, device_ids in query.items():
+            if not self.store.get_if_app_services_interested_in_user(user_id):
+                continue
+
+            # Find the associated appservice.
+            for service in services:
+                if service.is_exclusive_user(user_id):
+                    query_by_appservice.setdefault(service.id, {})[user_id] = (
+                        device_ids or []
+                    )
+                    continue
+
+        # Query each service in parallel.
+        results = await make_deferred_yieldable(
+            defer.DeferredList(
+                [
+                    run_in_background(
+                        self.appservice_api.query_keys,
+                        # We know this must be an app service.
+                        self.store.get_app_service_by_id(service_id),  # type: ignore[arg-type]
+                        service_query,
+                    )
+                    for service_id, service_query in query_by_appservice.items()
+                ],
+                consumeErrors=True,
+            )
+        )
+
+        # Patch together the results -- they are all independent (since they
+        # require exclusive control over the users). They get returned as a single
+        # dictionary.
+        key_queries: Dict[str, Dict[str, Dict[str, JsonDict]]] = {}
+        for success, result in results:
+            if success:
+                key_queries.update(result)
+
+        return key_queries
diff --git a/synapse/handlers/e2e_keys.py b/synapse/handlers/e2e_keys.py
index 9e7c2c45b557..007366747014 100644
--- a/synapse/handlers/e2e_keys.py
+++ b/synapse/handlers/e2e_keys.py
@@ -91,6 +91,9 @@ def __init__(self, hs: "HomeServer"):
         self._query_appservices_for_otks = (
             hs.config.experimental.msc3983_appservice_otk_claims
         )
+        self._query_appservices_for_keys = (
+            hs.config.experimental.msc3984_appservice_key_query
+        )
 
     @trace
     @cancellable
@@ -497,6 +500,19 @@ async def query_local_devices(
             local_query, include_displaynames
         )
 
+        # Check if the application services have any additional results.
+        if self._query_appservices_for_keys:
+            # Query the appservices for any keys.
+            appservice_results = await self._appservice_handler.query_keys(query)
+
+            # Merge results, overriding with what the appservice returned.
+            for user_id, devices in appservice_results.get("device_keys", {}).items():
+                # Copy the appservice device info over the homeserver device info, but
+                # don't completely overwrite it.
+                results.setdefault(user_id, {}).update(devices)
+
+            # TODO Handle cross-signing keys.
+
         # Build the result structure
         for user_id, device_keys in results.items():
             for device_id, device_info in device_keys.items():
diff --git a/tests/handlers/test_e2e_keys.py b/tests/handlers/test_e2e_keys.py
index 4ff04fc66bb7..2bc18f548b05 100644
--- a/tests/handlers/test_e2e_keys.py
+++ b/tests/handlers/test_e2e_keys.py
@@ -1015,3 +1015,122 @@ def test_query_appservice(self) -> None:
                 },
             },
         )
+
+    @override_config({"experimental_features": {"msc3984_appservice_key_query": True}})
+    def test_query_local_devices_appservice(self) -> None:
+        """Test that querying of appservices for keys overrides responses from the database."""
+        local_user = "@boris:" + self.hs.hostname
+        device_1 = "abc"
+        device_2 = "def"
+        device_3 = "ghi"
+
+        # There are 3 devices:
+        #
+        # 1. One which is uploaded to the homeserver.
+        # 2. One which is uploaded to the homeserver, but a newer copy is returned
+        #     by the appservice.
+        # 3. One which is only returned by the appservice.
+        device_key_1: JsonDict = {
+            "user_id": local_user,
+            "device_id": device_1,
+            "algorithms": [
+                "m.olm.curve25519-aes-sha2",
+                RoomEncryptionAlgorithms.MEGOLM_V1_AES_SHA2,
+            ],
+            "keys": {
+                "ed25519:abc": "base64+ed25519+key",
+                "curve25519:abc": "base64+curve25519+key",
+            },
+            "signatures": {local_user: {"ed25519:abc": "base64+signature"}},
+        }
+        device_key_2a: JsonDict = {
+            "user_id": local_user,
+            "device_id": device_2,
+            "algorithms": [
+                "m.olm.curve25519-aes-sha2",
+                RoomEncryptionAlgorithms.MEGOLM_V1_AES_SHA2,
+            ],
+            "keys": {
+                "ed25519:def": "base64+ed25519+key",
+                "curve25519:def": "base64+curve25519+key",
+            },
+            "signatures": {local_user: {"ed25519:def": "base64+signature"}},
+        }
+
+        device_key_2b: JsonDict = {
+            "user_id": local_user,
+            "device_id": device_2,
+            "algorithms": [
+                "m.olm.curve25519-aes-sha2",
+                RoomEncryptionAlgorithms.MEGOLM_V1_AES_SHA2,
+            ],
+            # The device ID is the same (above), but the keys are different.
+            "keys": {
+                "ed25519:xyz": "base64+ed25519+key",
+                "curve25519:xyz": "base64+curve25519+key",
+            },
+            "signatures": {local_user: {"ed25519:xyz": "base64+signature"}},
+        }
+        device_key_3: JsonDict = {
+            "user_id": local_user,
+            "device_id": device_3,
+            "algorithms": [
+                "m.olm.curve25519-aes-sha2",
+                RoomEncryptionAlgorithms.MEGOLM_V1_AES_SHA2,
+            ],
+            "keys": {
+                "ed25519:jkl": "base64+ed25519+key",
+                "curve25519:jkl": "base64+curve25519+key",
+            },
+            "signatures": {local_user: {"ed25519:jkl": "base64+signature"}},
+        }
+
+        # Upload keys for devices 1 & 2a.
+        self.get_success(
+            self.handler.upload_keys_for_user(
+                local_user, device_1, {"device_keys": device_key_1}
+            )
+        )
+        self.get_success(
+            self.handler.upload_keys_for_user(
+                local_user, device_2, {"device_keys": device_key_2a}
+            )
+        )
+
+        # Inject an appservice interested in this user.
+        appservice = ApplicationService(
+            token="i_am_an_app_service",
+            id="1234",
+            namespaces={"users": [{"regex": r"@boris:*", "exclusive": True}]},
+            # Note: this user does not have to match the regex above
+            sender="@as_main:test",
+        )
+        self.hs.get_datastores().main.services_cache = [appservice]
+        self.hs.get_datastores().main.exclusive_user_regex = _make_exclusive_regex(
+            [appservice]
+        )
+
+        # Setup a response.
+        self.appservice_api.query_keys.return_value = make_awaitable(
+            {
+                "device_keys": {
+                    local_user: {device_2: device_key_2b, device_3: device_key_3}
+                }
+            }
+        )
+
+        # Request all devices.
+        res = self.get_success(self.handler.query_local_devices({local_user: None}))
+        self.assertIn(local_user, res)
+        for res_key in res[local_user].values():
+            res_key.pop("unsigned", None)
+        self.assertDictEqual(
+            res,
+            {
+                local_user: {
+                    device_1: device_key_1,
+                    device_2: device_key_2b,
+                    device_3: device_key_3,
+                }
+            },
+        )