diff --git a/app/assets/stylesheets/components/message.scss b/app/assets/stylesheets/components/message.scss
index ec44dd8a7..47ee96790 100644
--- a/app/assets/stylesheets/components/message.scss
+++ b/app/assets/stylesheets/components/message.scss
@@ -5,11 +5,19 @@
     margin: 0;
 
     a {
-      display: block;
+      display: inline-block;
       margin-bottom: -$gutter;
       padding-bottom: $gutter;
     }
 
+    &-separator {
+      display: inline-block;
+      vertical-align: top;
+      color: $secondary-text-colour;
+      padding: 0 4px 0 5px;
+      font-weight: normal;
+    }
+
   }
 
   &-type {
@@ -44,7 +52,7 @@
 
   &-folder {
 
-    a {
+    a:first-child {
       text-indent: 40px;
       background-image: file-url('folder-blue-bold.svg');
       background-repeat: no-repeat;
diff --git a/app/templates/views/templates/_template_list.html b/app/templates/views/templates/_template_list.html
index 53439904a..e4fe60476 100644
--- a/app/templates/views/templates/_template_list.html
+++ b/app/templates/views/templates/_template_list.html
@@ -12,7 +12,7 @@
 {% else %}
   <nav id=template-list>
     {% for item in template_list %}
-      <div class="template-list-item {% if can_manage_folders %}template-list-item-with-checkbox{% endif %}">
+      <div class="template-list-item {% if can_manage_folders %}template-list-item-with-checkbox{% endif %} {% if item.ancestors %}template-list-item-hidden-by-default{% endif %}">
         {% if can_manage_folders %}
           {{ unlabelled_checkbox(
             id='templates-or-folder-{}'.format(item.id),
@@ -20,17 +20,22 @@
             value=item.id,
           ) }}
         {% endif %}
-        {% if item.is_folder %}
-          <h2 class="message-name template-list-folder">
+        <h2 class="message-name {% if item.is_folder or (item.ancestors and not item.is_folder) %}template-list-folder{% endif %}">
+          {% for ancestor in item.ancestors %}
+            <a href="{{ url_for('.choose_template', service_id=current_service.id, template_type=template_type, template_folder_id=ancestor.id) }}">
+              {{ ancestor.name }}
+            </a> <span class="message-name-separator">/</span>
+          {% endfor %}
+          {% if item.is_folder %}
             <a href="{{ url_for('.choose_template', service_id=current_service.id, template_type=template_type, template_folder_id=item.id) }}">
               {{ item.name }}
             </a>
-          </h2>
-        {% else %}
-          <h2 class="message-name">
-            <a href="{{ url_for('.view_template', service_id=current_service.id, template_id=item.id) }}">{{ item.name }}</a>
-          </h2>
-        {% endif %}
+          {% else %}
+            <a href="{{ url_for('.view_template', service_id=current_service.id, template_id=item.id) }}">
+              {{ item.name }}
+            </a>
+          {% endif %}
+        </h2>
         <p class="message-type">
           {{ item.hint }}
         </p>
diff --git a/tests/app/main/views/test_template_folders.py b/tests/app/main/views/test_template_folders.py
index 323c461e7..fd452b3a5 100644
--- a/tests/app/main/views/test_template_folders.py
+++ b/tests/app/main/views/test_template_folders.py
@@ -118,11 +118,11 @@ def test_post_add_template_folder_page(client_request, service_one, mocker, pare
             ['Text message', 'Email', 'Letter'],
             [
                 'folder_one 2 folders',
-                'folder_one_one 1 template, 1 folder',
-                'folder_one_one_one 1 template',
-                'sms_template_nested Text message template',
-                'letter_template_nested Letter template',
-                'folder_one_two Empty',
+                'folder_one / folder_one_one 1 template, 1 folder',
+                'folder_one / folder_one_one / folder_one_one_one 1 template',
+                'folder_one / folder_one_one / folder_one_one_one / sms_template_nested Text message template',
+                'folder_one / folder_one_one / letter_template_nested Letter template',
+                'folder_one / folder_one_two Empty',
                 'folder_two Empty',
                 'sms_template_one Text message template',
                 'sms_template_two Text message template',
@@ -141,9 +141,9 @@ def test_post_add_template_folder_page(client_request, service_one, mocker, pare
             ['All', 'Email', 'Letter'],
             [
                 'folder_one 1 folder',
-                'folder_one_one 1 folder',
-                'folder_one_one_one 1 template',
-                'sms_template_nested Text message template',
+                'folder_one / folder_one_one 1 folder',
+                'folder_one / folder_one_one / folder_one_one_one 1 template',
+                'folder_one / folder_one_one / folder_one_one_one / sms_template_nested Text message template',
                 'sms_template_one Text message template',
                 'sms_template_two Text message template',
             ],
@@ -157,9 +157,9 @@ def test_post_add_template_folder_page(client_request, service_one, mocker, pare
             ['Text message', 'Email', 'Letter'],
             [
                 'folder_one_one 1 template, 1 folder',
-                'folder_one_one_one 1 template',
-                'sms_template_nested Text message template',
-                'letter_template_nested Letter template',
+                'folder_one_one / folder_one_one_one 1 template',
+                'folder_one_one / folder_one_one_one / sms_template_nested Text message template',
+                'folder_one_one / letter_template_nested Letter template',
                 'folder_one_two Empty',
             ],
             None,
@@ -172,8 +172,8 @@ def test_post_add_template_folder_page(client_request, service_one, mocker, pare
             ['All', 'Email', 'Letter'],
             [
                 'folder_one_one 1 folder',
-                'folder_one_one_one 1 template',
-                'sms_template_nested Text message template',
+                'folder_one_one / folder_one_one_one 1 template',
+                'folder_one_one / folder_one_one_one / sms_template_nested Text message template',
             ],
             None,
         ),
@@ -194,7 +194,7 @@ def test_post_add_template_folder_page(client_request, service_one, mocker, pare
             ['Text message', 'Email', 'Letter'],
             [
                 'folder_one_one_one 1 template',
-                'sms_template_nested Text message template',
+                'folder_one_one_one / sms_template_nested Text message template',
                 'letter_template_nested Letter template',
             ],
             None,