diff --git a/lms/djangoapps/courseware/module_render.py b/lms/djangoapps/courseware/module_render.py
index 04015787c6f1..07d22c465230 100644
--- a/lms/djangoapps/courseware/module_render.py
+++ b/lms/djangoapps/courseware/module_render.py
@@ -29,6 +29,7 @@
 from edx_proctoring.api import get_attempt_status_summary
 from edx_proctoring.services import ProctoringService
 from edx_rest_framework_extensions.auth.jwt.authentication import JwtAuthentication
+from edx_rest_framework_extensions.permissions import JwtRestrictedApplication
 from edx_when.field_data import DateLookupFieldData
 from eventtracking import tracker
 from opaque_keys import InvalidKeyError
@@ -944,12 +945,19 @@ def handle_xblock_callback(request, course_id, usage_id, handler, suffix=None):
                 )
             else:
                 if user_auth_tuple is not None:
-                    request.user, _ = user_auth_tuple
+                    # When using JWT authentication, the second element contains the JWT token. We need it to determine
+                    # whether the application that issued the token is restricted.
+                    request.user, request.auth = user_auth_tuple
+                    # This is verified by the `JwtRestrictedApplication` before it decodes the token.
+                    request.successful_authenticator = authenticator
                     break
 
     # NOTE (CCB): Allow anonymous GET calls (e.g. for transcripts). Modifying this view is simpler than updating
     # the XBlocks to use `handle_xblock_callback_noauth`, which is practically identical to this view.
-    if request.method != 'GET' and not (request.user and request.user.is_authenticated):
+    # Block all request types coming from restricted applications.
+    if (
+        request.method != 'GET' and not (request.user and request.user.is_authenticated)
+    ) or JwtRestrictedApplication().has_permission(request, None):  # type: ignore
         return HttpResponseForbidden('Unauthenticated')
 
     request.user.known = request.user.is_authenticated
diff --git a/lms/djangoapps/courseware/tests/test_module_render.py b/lms/djangoapps/courseware/tests/test_module_render.py
index 9e187fd1ebe2..ea22027c8c04 100644
--- a/lms/djangoapps/courseware/tests/test_module_render.py
+++ b/lms/djangoapps/courseware/tests/test_module_render.py
@@ -81,7 +81,7 @@
 from lms.djangoapps.lms_xblock.field_data import LmsFieldData
 from openedx.core.djangoapps.credit.api import set_credit_requirement_status, set_credit_requirements
 from openedx.core.djangoapps.credit.models import CreditCourse
-from openedx.core.djangoapps.oauth_dispatch.jwt import create_jwt_for_user
+from openedx.core.djangoapps.oauth_dispatch.jwt import _create_jwt, create_jwt_for_user
 from openedx.core.djangoapps.oauth_dispatch.tests.factories import AccessTokenFactory, ApplicationFactory
 from openedx.core.lib.courses import course_image_url
 from openedx.core.lib.gating import api as gating_api
@@ -375,6 +375,26 @@ def test_jwt_authentication(self):
         response = self.client.post(dispatch_url, {}, **headers)
         assert 200 == response.status_code
 
+    def test_jwt_authentication_with_restricted_application(self):
+        """Test that the XBlock endpoint disallows JWT authentication with restricted applications."""
+
+        def _mock_create_restricted_jwt(*args, **kwargs):
+            """Pass an additional argument to `_create_jwt` without modifying the signature of `create_jwt_for_user`."""
+            kwargs['is_restricted'] = True
+            return _create_jwt(*args, **kwargs)
+
+        with patch('openedx.core.djangoapps.oauth_dispatch.jwt._create_jwt', _mock_create_restricted_jwt):
+            token = create_jwt_for_user(self.mock_user)
+
+        dispatch_url = self._get_dispatch_url()
+        headers = {'HTTP_AUTHORIZATION': 'JWT ' + token}
+
+        response = self.client.get(dispatch_url, {}, **headers)
+        assert 403 == response.status_code
+
+        response = self.client.post(dispatch_url, {}, **headers)
+        assert 403 == response.status_code
+
     def test_missing_position_handler(self):
         """
         Test that sending POST request without or invalid position argument don't raise server error