diff --git a/awx/api/views.py b/awx/api/views.py
index b1ca33ed27..091262964e 100644
--- a/awx/api/views.py
+++ b/awx/api/views.py
@@ -543,7 +543,12 @@ class AuthTokenView(APIView):
                                                 token_key=t.key)
                     t.invalidate(reason='limit_reached')
 
-            return Response({'token': token.key, 'expires': token.expires})
+            # Note: This header is normally added in the middleware whenever an
+            # auth token is included in the request header.
+            headers = {
+                'Auth-Token-Timeout': int(settings.AUTH_TOKEN_EXPIRATION)
+            }
+            return Response({'token': token.key, 'expires': token.expires}, headers=headers)
         return Response(serializer.errors, status=status.HTTP_400_BAD_REQUEST)
 
 class OrganizationList(ListCreateAPIView):