diff --git a/changelog.d/10593.bugfix b/changelog.d/10593.bugfix
new file mode 100644
index 000000000..492e58a7a
--- /dev/null
+++ b/changelog.d/10593.bugfix
@@ -0,0 +1 @@
+Reject Client-Server /keys/query requests which provide device_ids incorrectly.
\ No newline at end of file
diff --git a/synapse/api/errors.py b/synapse/api/errors.py
index dc662bca8..9480f448d 100644
--- a/synapse/api/errors.py
+++ b/synapse/api/errors.py
@@ -147,6 +147,14 @@ class SynapseError(CodeMessageException):
         return cs_error(self.msg, self.errcode)
 
 
+class InvalidAPICallError(SynapseError):
+    """You called an existing API endpoint, but fed that endpoint
+    invalid or incomplete data."""
+
+    def __init__(self, msg: str):
+        super().__init__(HTTPStatus.BAD_REQUEST, msg, Codes.BAD_JSON)
+
+
 class ProxiedRequestError(SynapseError):
     """An error from a general matrix endpoint, eg. from a proxied Matrix API call.
 
diff --git a/synapse/rest/client/keys.py b/synapse/rest/client/keys.py
index d0d9d30d4..012491f59 100644
--- a/synapse/rest/client/keys.py
+++ b/synapse/rest/client/keys.py
@@ -15,8 +15,9 @@
 # limitations under the License.
 
 import logging
+from typing import Any
 
-from synapse.api.errors import SynapseError
+from synapse.api.errors import InvalidAPICallError, SynapseError
 from synapse.http.servlet import (
     RestServlet,
     parse_integer,
@@ -163,6 +164,19 @@ class KeyQueryServlet(RestServlet):
         device_id = requester.device_id
         timeout = parse_integer(request, "timeout", 10 * 1000)
         body = parse_json_object_from_request(request)
+
+        device_keys = body.get("device_keys")
+        if not isinstance(device_keys, dict):
+            raise InvalidAPICallError("'device_keys' must be a JSON object")
+
+        def is_list_of_strings(values: Any) -> bool:
+            return isinstance(values, list) and all(isinstance(v, str) for v in values)
+
+        if any(not is_list_of_strings(keys) for keys in device_keys.values()):
+            raise InvalidAPICallError(
+                "'device_keys' values must be a list of strings",
+            )
+
         result = await self.e2e_keys_handler.query_devices(
             body, timeout, user_id, device_id
         )
diff --git a/tests/rest/client/v2_alpha/test_keys.py b/tests/rest/client/v2_alpha/test_keys.py
new file mode 100644
index 000000000..80a4e728f
--- /dev/null
+++ b/tests/rest/client/v2_alpha/test_keys.py
@@ -0,0 +1,77 @@
+from http import HTTPStatus
+
+from synapse.api.errors import Codes
+from synapse.rest import admin
+from synapse.rest.client import keys, login
+
+from tests import unittest
+
+
+class KeyQueryTestCase(unittest.HomeserverTestCase):
+    servlets = [
+        keys.register_servlets,
+        admin.register_servlets_for_client_rest_resource,
+        login.register_servlets,
+    ]
+
+    def test_rejects_device_id_ice_key_outside_of_list(self):
+        self.register_user("alice", "wonderland")
+        alice_token = self.login("alice", "wonderland")
+        bob = self.register_user("bob", "uncle")
+        channel = self.make_request(
+            "POST",
+            "/_matrix/client/r0/keys/query",
+            {
+                "device_keys": {
+                    bob: "device_id1",
+                },
+            },
+            alice_token,
+        )
+        self.assertEqual(channel.code, HTTPStatus.BAD_REQUEST, channel.result)
+        self.assertEqual(
+            channel.json_body["errcode"],
+            Codes.BAD_JSON,
+            channel.result,
+        )
+
+    def test_rejects_device_key_given_as_map_to_bool(self):
+        self.register_user("alice", "wonderland")
+        alice_token = self.login("alice", "wonderland")
+        bob = self.register_user("bob", "uncle")
+        channel = self.make_request(
+            "POST",
+            "/_matrix/client/r0/keys/query",
+            {
+                "device_keys": {
+                    bob: {
+                        "device_id1": True,
+                    },
+                },
+            },
+            alice_token,
+        )
+
+        self.assertEqual(channel.code, HTTPStatus.BAD_REQUEST, channel.result)
+        self.assertEqual(
+            channel.json_body["errcode"],
+            Codes.BAD_JSON,
+            channel.result,
+        )
+
+    def test_requires_device_key(self):
+        """`device_keys` is required. We should complain if it's missing."""
+        self.register_user("alice", "wonderland")
+        alice_token = self.login("alice", "wonderland")
+        channel = self.make_request(
+            "POST",
+            "/_matrix/client/r0/keys/query",
+            {},
+            alice_token,
+        )
+        self.assertEqual(channel.code, HTTPStatus.BAD_REQUEST, channel.result)
+        self.assertEqual(
+            channel.json_body["errcode"],
+            Codes.BAD_JSON,
+            channel.result,
+        )