diff --git a/app/assets/stylesheets/components/message.scss b/app/assets/stylesheets/components/message.scss
index 55267d554..2e9b52180 100644
--- a/app/assets/stylesheets/components/message.scss
+++ b/app/assets/stylesheets/components/message.scss
@@ -55,3 +55,59 @@
   }
 
 }
+
+.folder-heading {
+
+  .column-main>.grid-row:first-child &.heading-medium {
+    margin-top: 18px;
+  }
+
+  overflow: hidden;
+  text-overflow: ellipsis;
+  white-space: nowrap;
+
+
+  a,
+  &-folder {
+
+    display: inline-block;
+    vertical-align: top;
+    padding: 5px 0 0 60px;
+    background-repeat: no-repeat;
+    background-size: 38px auto;
+    background-position: 0 1px;
+
+  }
+
+  a {
+
+    background-image: file-url('folder-blue.svg');
+    max-width: 33%;
+    overflow: hidden;
+    text-overflow: ellipsis;
+
+  }
+
+  &-folder {
+
+    padding-left: 0;
+
+    &:first-child {
+      background-image: file-url('folder-black.svg');
+      padding-left: $gutter * 2;
+    }
+
+  }
+
+  &-separator {
+
+    display: inline-block;
+    vertical-align: top;
+    color: $secondary-text-colour;
+    padding: 5px 4px 0 5px;
+    font-weight: normal;
+
+  }
+
+
+}
diff --git a/app/models/service.py b/app/models/service.py
index 32de656ba..d91a12e5e 100644
--- a/app/models/service.py
+++ b/app/models/service.py
@@ -316,6 +316,12 @@ class Service():
         ]
 
     def get_template_folder(self, folder_id):
+        if folder_id is None:
+            return {
+                'id': None,
+                'name': 'Templates',
+                'parent_id': None,
+            }
         return self._get_by_id(self.all_template_folders, folder_id)
 
     def is_folder_visible(self, template_folder_id, template_type='all'):
@@ -335,19 +341,16 @@ class Service():
         return False
 
     def get_template_folder_path(self, template_folder_id):
-        if template_folder_id is None:
-            return []
 
-        id_to_folder = {folder['id']: folder for folder in self.all_template_folders}
+        folder = self.get_template_folder(template_folder_id)
 
-        folder = id_to_folder[template_folder_id]
-        path = [folder]
+        if folder['id'] is None:
+            return [folder]
 
-        while folder['parent_id']:
-            folder = id_to_folder[folder['parent_id']]
-            path.append(folder)
-
-        return list(reversed(path))
+        return [
+            self.get_template_folder(folder['parent_id']),
+            folder,
+        ]
 
     def get_template_folders_and_templates(self, template_type, template_folder_id):
         return (
diff --git a/app/templates/components/folder-path.html b/app/templates/components/folder-path.html
new file mode 100644
index 000000000..ef747046b
--- /dev/null
+++ b/app/templates/components/folder-path.html
@@ -0,0 +1,50 @@
+{% macro folder_path(
+  folders,
+  service_id,
+  template_type,
+  fallback_page_title=None,
+  show_fallback_page_title=False
+) %}
+  {% if show_fallback_page_title %}
+    <h1 class="heading-large">
+      {{ fallback_page_title }}
+    </h1>
+  {% else %}
+    <h1 class="heading-medium folder-heading">
+      {% for folder in folders %}
+        {% if loop.last %}
+          <span class="folder-heading-folder">{{ folder.name }}</span>
+        {% else %}
+          {% if folder.id %}
+            <a href="{{ url_for('.choose_template', service_id=service_id, template_type=template_type, template_folder_id=folder.id) }}">{{ folder.name }}</a> {{ folder_path_separator() }}
+          {% else %}
+            <a href="{{ url_for('.choose_template', service_id=service_id, template_type=template_type) }}">Templates</a> {{ folder_path_separator() }}
+          {% endif %}
+        {% endif %}
+      {% endfor %}
+    </h1>
+  {% endif %}
+{% endmacro %}
+
+
+{% macro page_title_folder_path(
+  folders,
+  fallback_page_title=None,
+  show_fallback_page_title=False
+) %}
+  {% if show_fallback_page_title %}
+    {{ fallback_page_title }}
+  {% else %}
+    {% for folder in folders|reverse %}
+      {{ folder.name }}
+      {% if not loop.last %}
+        –
+      {% endif %}
+    {% endfor %}
+  {% endif %}
+{% endmacro %}
+
+
+{% macro folder_path_separator() %}
+  <span class="folder-heading-separator">/</span>
+{% endmacro %}
diff --git a/app/templates/views/templates/choose.html b/app/templates/views/templates/choose.html
index c3e519c6d..9b5e8fe6c 100644
--- a/app/templates/views/templates/choose.html
+++ b/app/templates/views/templates/choose.html
@@ -1,3 +1,4 @@
+{% from "components/folder-path.html" import folder_path, page_title_folder_path %}
 {% from "components/pill.html" import pill %}
 {% from "components/message-count-label.html" import message_count_label %}
 {% from "components/textbox.html" import textbox %}
@@ -8,10 +9,11 @@
 {% set page_title = 'Templates' %}
 
 {% block service_page_title %}
-  {{ page_title }}
-  {% for folder in template_folder_path %}
-    / {{ folder.name }}
-  {% endfor %}
+  {{ page_title_folder_path(
+    template_folder_path,
+    fallback_page_title=page_title,
+    show_fallback_page_title=not current_service.all_template_folders
+  ) }}
 {% endblock %}
 
 {% block maincolumn_content %}
@@ -46,27 +48,19 @@
 
     <div class="grid-row bottom-gutter-2-3">
       <div class="column-two-thirds">
-        <h1 class="heading-large">
-          {% if template_folder_path %}
-            <a href="{{ url_for('.choose_template', service_id=current_service.id, template_type=template_type) }}">{{ page_title }}</a>
-          {% else %}
-            {{ page_title }}
-          {% endif %}
-          {% for folder in template_folder_path %}
-            /
-            {% if loop.last %}
-              {{ folder.name }}
-            {% else %}
-              <a href="{{ url_for('.choose_template', service_id=current_service.id, template_type=template_type, template_folder_id=folder.id) }}">{{ folder.name }}</a>
-            {% endif %}
-          {% endfor %}
-        </h1>
+        {{ folder_path(
+          folders=template_folder_path,
+          service_id=current_service.id,
+          template_type=template_type,
+          fallback_page_title=page_title,
+          show_fallback_page_title=not current_service.all_template_folders
+        ) }}
       </div>
       {% if current_user.has_permissions('manage_templates') %}
         <div class="column-one-third">
           <a href="{{ url_for('.add_template_by_type', service_id=current_service.id, template_folder_id=current_template_folder_id) }}" class="button align-with-heading">Add new template</a>
 
-        {% if can_manage_folders and template_folder_path %}
+        {% if can_manage_folders and current_template_folder_id %}
           <a href="{{ url_for('.manage_template_folder', service_id=current_service.id, template_folder_id=current_template_folder_id) }}" class="align-with-heading">Manage</a>
         {% endif %}
         </div>
diff --git a/tests/app/main/views/test_template_folders.py b/tests/app/main/views/test_template_folders.py
index 8fe03eb91..f1dd42de0 100644
--- a/tests/app/main/views/test_template_folders.py
+++ b/tests/app/main/views/test_template_folders.py
@@ -99,10 +99,19 @@ def test_post_add_template_folder_page(client_request, service_one, mocker, pare
 
 
 @pytest.mark.parametrize(
-    'expected_page_title, extra_args, expected_nav_links, expected_items',
+    (
+        'expected_title_tag,'
+        'expected_page_title,'
+        'expected_parent_link_args,'
+        'extra_args,'
+        'expected_nav_links,'
+        'expected_items'
+    ),
     [
         (
+            'Templates – service one – GOV.UK Notify',
             'Templates',
+            None,
             {},
             ['Text message', 'Email', 'Letter'],
             [
@@ -117,7 +126,9 @@ def test_post_add_template_folder_page(client_request, service_one, mocker, pare
             ]
         ),
         (
+            'Templates – service one – GOV.UK Notify',
             'Templates',
+            None,
             {'template_type': 'sms'},
             ['All', 'Email', 'Letter'],
             [
@@ -127,7 +138,9 @@ def test_post_add_template_folder_page(client_request, service_one, mocker, pare
             ],
         ),
         (
+            'folder_one – Templates – service one – GOV.UK Notify',
             'Templates / folder_one',
+            {'template_type': 'all'},
             {'template_folder_id': PARENT_FOLDER_ID},
             ['Text message', 'Email', 'Letter'],
             [
@@ -136,7 +149,9 @@ def test_post_add_template_folder_page(client_request, service_one, mocker, pare
             ],
         ),
         (
+            'folder_one – Templates – service one – GOV.UK Notify',
             'Templates / folder_one',
+            {'template_type': 'sms'},
             {'template_type': 'sms', 'template_folder_id': PARENT_FOLDER_ID},
             ['All', 'Email', 'Letter'],
             [
@@ -144,13 +159,17 @@ def test_post_add_template_folder_page(client_request, service_one, mocker, pare
             ],
         ),
         (
+            'folder_one – Templates – service one – GOV.UK Notify',
             'Templates / folder_one',
+            {'template_type': 'email'},
             {'template_type': 'email', 'template_folder_id': PARENT_FOLDER_ID},
             ['All', 'Text message', 'Letter'],
             [],
         ),
         (
-            'Templates / folder_one / folder_one_one',
+            'folder_one_one – folder_one – service one – GOV.UK Notify',
+            'folder_one / folder_one_one',
+            {'template_type': 'all', 'template_folder_id': PARENT_FOLDER_ID},
             {'template_folder_id': CHILD_FOLDER_ID},
             ['Text message', 'Email', 'Letter'],
             [
@@ -159,7 +178,9 @@ def test_post_add_template_folder_page(client_request, service_one, mocker, pare
             ],
         ),
         (
-            'Templates / folder_one / folder_one_one / folder_one_one_one',
+            'folder_one_one_one – folder_one_one – service one – GOV.UK Notify',
+            'folder_one_one / folder_one_one_one',
+            {'template_type': 'all', 'template_folder_id': CHILD_FOLDER_ID},
             {'template_folder_id': GRANDCHILD_FOLDER_ID},
             ['Text message', 'Email', 'Letter'],
             [
@@ -175,7 +196,9 @@ def test_should_show_templates_folder_page(
     service_one,
     mocker,
     fake_uuid,
+    expected_title_tag,
     expected_page_title,
+    expected_parent_link_args,
     extra_args,
     expected_nav_links,
     expected_items,
@@ -206,11 +229,23 @@ def test_should_show_templates_folder_page(
     page = client_request.get(
         'main.choose_template',
         service_id=SERVICE_ONE_ID,
+        _test_page_title=False,
         **extra_args
     )
 
+    assert normalize_spaces(page.select_one('title').text) == expected_title_tag
     assert normalize_spaces(page.select_one('h1').text) == expected_page_title
 
+    if expected_parent_link_args:
+        assert len(page.select('h1 a')) == 1
+        assert page.select_one('h1 a')['href'] == url_for(
+            'main.choose_template',
+            service_id=SERVICE_ONE_ID,
+            **expected_parent_link_args
+        )
+    else:
+        assert page.select_one('h1 a') is None
+
     links_in_page = page.select('.pill a')
 
     assert len(links_in_page) == len(expected_nav_links)
@@ -312,7 +347,11 @@ def test_can_create_email_template_with_parent_folder(
         data['parent_folder_id'])
 
 
-def test_get_manage_folder_page(client_request, service_one, mock_get_template_folders):
+def test_get_manage_folder_page(
+    client_request,
+    service_one,
+    mock_get_template_folders,
+):
     folder_id = str(uuid.uuid4())
     mock_get_template_folders.return_value = [
         {'id': folder_id, 'name': 'folder_two', 'parent_id': None},