diff --git a/app/template/rest.py b/app/template/rest.py
index 56416dc30..8cbb4125f 100644
--- a/app/template/rest.py
+++ b/app/template/rest.py
@@ -12,6 +12,7 @@ from notifications_utils import SMS_CHAR_COUNT_LIMIT
 from notifications_utils.pdf import extract_page_from_pdf
 from notifications_utils.template import SMSMessageTemplate
 from requests import post as requests_post
+from sqlalchemy.orm.exc import NoResultFound
 
 from app.dao.notifications_dao import get_notification_by_id
 from app.dao.services_dao import dao_fetch_service_by_id
@@ -51,8 +52,13 @@ def _content_count_greater_than_limit(content, template_type):
 
 def validate_parent_folder(template_json):
     if template_json.get("parent_folder_id"):
-        return dao_get_template_folder_by_id_and_service_id(template_folder_id=template_json.pop("parent_folder_id"),
-                                                            service_id=template_json['service'])
+        try:
+            return dao_get_template_folder_by_id_and_service_id(
+                template_folder_id=template_json.pop("parent_folder_id"),
+                service_id=template_json['service']
+            )
+        except NoResultFound:
+            raise InvalidRequest("parent_folder_id not found", status_code=400)
     else:
         return None
 
diff --git a/tests/app/template/test_rest.py b/tests/app/template/test_rest.py
index d3de8e3d5..7cf46aa80 100644
--- a/tests/app/template/test_rest.py
+++ b/tests/app/template/test_rest.py
@@ -107,7 +107,7 @@ def test_should_create_a_new_template_for_a_service_adds_folder_relationship(
     assert template.folder == parent_folder
 
 
-def test_create_template_should_return_404_if_folder_is_for_a_different_service(
+def test_create_template_should_return_400_if_folder_is_for_a_different_service(
         client, sample_service
 ):
     service2 = create_service(service_name='second service')
@@ -129,10 +129,11 @@ def test_create_template_should_return_404_if_folder_is_for_a_different_service(
         headers=[('Content-Type', 'application/json'), auth_header],
         data=data
     )
-    assert response.status_code == 404
+    assert response.status_code == 400
+    assert json.loads(response.get_data(as_text=True))['message'] == 'parent_folder_id not found'
 
 
-def test_create_template_should_return_404_if_folder_does_not_exist(
+def test_create_template_should_return_400_if_folder_does_not_exist(
         client, sample_service
 ):
     data = {
@@ -151,7 +152,8 @@ def test_create_template_should_return_404_if_folder_does_not_exist(
         headers=[('Content-Type', 'application/json'), auth_header],
         data=data
     )
-    assert response.status_code == 404
+    assert response.status_code == 400
+    assert json.loads(response.get_data(as_text=True))['message'] == 'parent_folder_id not found'
 
 
 def test_should_raise_error_if_service_does_not_exist_on_create(client, sample_user, fake_uuid):