diff --git a/awx/api/views/__init__.py b/awx/api/views/__init__.py
index fe116afb984f..20515a69c8a0 100644
--- a/awx/api/views/__init__.py
+++ b/awx/api/views/__init__.py
@@ -2392,6 +2392,14 @@ class JobTemplateList(ListCreateAPIView):
     serializer_class = serializers.JobTemplateSerializer
     always_allow_superuser = False
 
+    def check_permissions(self, request):
+        if request.method == 'POST':
+            can_access, messages = request.user.can_access_with_errors(self.model, 'add', request.data)
+            if not can_access:
+                self.permission_denied(request, message=messages)
+
+        super(JobTemplateList, self).check_permissions(request)
+
 
 class JobTemplateDetail(RelatedJobsPreventDeleteMixin, RetrieveUpdateDestroyAPIView):
     model = models.JobTemplate
diff --git a/awx/main/access.py b/awx/main/access.py
index ae39bba1b135..9748ddd8d3df 100644
--- a/awx/main/access.py
+++ b/awx/main/access.py
@@ -1595,6 +1595,8 @@ def get_value(Class, field):
         inventory = get_value(Inventory, 'inventory')
         if inventory:
             if self.user not in inventory.use_role:
+                if self.save_messages:
+                    self.messages['inventory'] = [_('You do not have use permission on Inventory')]
                 return False
 
         if not self.check_related('execution_environment', ExecutionEnvironment, data, role_field='read_role'):
@@ -1603,11 +1605,16 @@ def get_value(Class, field):
         project = get_value(Project, 'project')
         # If the user has admin access to the project (as an org admin), should
         # be able to proceed without additional checks.
-        if project:
-            return self.user in project.use_role
-        else:
+        if not project:
+            return False
+
+        if self.user not in project.use_role:
+            if self.save_messages:
+                self.messages['project'] = [_('You do not have use permission on Project')]
             return False
 
+        return True
+
     @check_superuser
     def can_copy_related(self, obj):
         """
diff --git a/awx/main/tests/functional/test_rbac_job_templates.py b/awx/main/tests/functional/test_rbac_job_templates.py
index 0b73dc34cb76..34f82d9a74b9 100644
--- a/awx/main/tests/functional/test_rbac_job_templates.py
+++ b/awx/main/tests/functional/test_rbac_job_templates.py
@@ -182,8 +182,14 @@ def test_job_template_creator_access(project, organization, rando, post, setup_m
 
 @pytest.mark.django_db
 @pytest.mark.job_permissions
-@pytest.mark.parametrize('lacking', ['project', 'inventory'])
-def test_job_template_insufficient_creator_permissions(lacking, project, inventory, organization, rando, post):
+@pytest.mark.parametrize(
+    'lacking,reason',
+    [
+        ('project', 'You do not have use permission on Project'),
+        ('inventory', 'You do not have use permission on Inventory'),
+    ],
+)
+def test_job_template_insufficient_creator_permissions(lacking, reason, project, inventory, organization, rando, post):
     if lacking != 'project':
         project.use_role.members.add(rando)
     else:
@@ -192,12 +198,13 @@ def test_job_template_insufficient_creator_permissions(lacking, project, invento
         inventory.use_role.members.add(rando)
     else:
         inventory.read_role.members.add(rando)
-    post(
+    response = post(
         url=reverse('api:job_template_list'),
         data=dict(name='newly-created-jt', inventory=inventory.id, project=project.pk, playbook='helloworld.yml'),
         user=rando,
         expect=403,
     )
+    assert reason in response.data[lacking]
 
 
 @pytest.mark.django_db