diff --git a/docs/overview/directory-structure.md b/docs/overview/directory-structure.md
index 8d4f3fea61..5cf83c7095 100644
--- a/docs/overview/directory-structure.md
+++ b/docs/overview/directory-structure.md
@@ -46,7 +46,7 @@ See [our docs](../subsystems/html-templates.html) for details on Zulip's
 templating systems.
 
 * `templates/zerver/` For [Jinja2](http://jinja.pocoo.org/) templates
-  for the backend (for zerver app).
+  for the backend (for zerver app; logged-in content is in `templates/zerver/app`).
 
 * `static/templates/` [Handlebars](http://handlebarsjs.com/) templates for the frontend.
 
diff --git a/docs/subsystems/html-templates.md b/docs/subsystems/html-templates.md
index 50576b7091..739925dbce 100644
--- a/docs/subsystems/html-templates.md
+++ b/docs/subsystems/html-templates.md
@@ -32,8 +32,8 @@ renders the template. For example, if you want to find the context
 passed to `index.html`, you can do:
 
 ```
-$ git grep zerver/index.html '*.py'
-zerver/views/home.py:    response = render(request, 'zerver/index.html',
+$ git grep zerver/app/index.html '*.py'
+zerver/views/home.py:    response = render(request, 'zerver/app/index.html',
 ```
 
 The next line in the code being the context definition.
diff --git a/docs/subsystems/markdown.md b/docs/subsystems/markdown.md
index da8840e7ed..dcbe9f9a20 100644
--- a/docs/subsystems/markdown.md
+++ b/docs/subsystems/markdown.md
@@ -100,7 +100,7 @@ places:
   your changes won't be supported in the frontend processor.
 * If desired, the typeahead logic in `static/js/composebox_typeahead.js`.
 * The test suite, probably via adding entries to `zerver/tests/fixtures/markdown_test_cases.json`.
-* The in-app markdown documentation (`templates/zerver/markdown_help.html`).
+* The in-app markdown documentation (`templates/zerver/app/markdown_help.html`).
 * The list of changes to markdown at the end of this document.
 
 Important considerations for any changes are:
diff --git a/docs/tutorials/new-feature-tutorial.md b/docs/tutorials/new-feature-tutorial.md
index 4c9817d5b5..2ccbf3ba14 100644
--- a/docs/tutorials/new-feature-tutorial.md
+++ b/docs/tutorials/new-feature-tutorial.md
@@ -121,7 +121,7 @@ feature requires UI changes, you may need to add additional CSS to this
 file.
 
 **Templates:** The initial page structure is rendered via Jinja2
-templates located in `templates/zerver`. For JavaScript, Zulip uses
+templates located in `templates/zerver/app`. For JavaScript, Zulip uses
 Handlebars templates located in `static/templates`. Templates are
 precompiled as part of the build/deploy process.
 
diff --git a/docs/tutorials/writing-views.md b/docs/tutorials/writing-views.md
index 1c8995d866..a9ce556c65 100644
--- a/docs/tutorials/writing-views.md
+++ b/docs/tutorials/writing-views.md
@@ -101,7 +101,7 @@ def home(request):
 ### Writing a template
 
 Templates for the main website are found in
-[templates/zerver](https://github.com/zulip/zulip/blob/master/templates/zerver).
+[templates/zerver/app](https://github.com/zulip/zulip/blob/master/templates/zerver/app).
 
 
 ## Writing API REST endpoints
diff --git a/templates/zerver/bankruptcy.html b/templates/zerver/app/bankruptcy.html
similarity index 100%
rename from templates/zerver/bankruptcy.html
rename to templates/zerver/app/bankruptcy.html
diff --git a/templates/zerver/compose.html b/templates/zerver/app/compose.html
similarity index 100%
rename from templates/zerver/compose.html
rename to templates/zerver/app/compose.html
diff --git a/templates/zerver/delete_message.html b/templates/zerver/app/delete_message.html
similarity index 100%
rename from templates/zerver/delete_message.html
rename to templates/zerver/app/delete_message.html
diff --git a/templates/zerver/deprecation_notice.html b/templates/zerver/app/deprecation_notice.html
similarity index 100%
rename from templates/zerver/deprecation_notice.html
rename to templates/zerver/app/deprecation_notice.html
diff --git a/templates/zerver/drafts.html b/templates/zerver/app/drafts.html
similarity index 100%
rename from templates/zerver/drafts.html
rename to templates/zerver/app/drafts.html
diff --git a/templates/zerver/home.html b/templates/zerver/app/home.html
similarity index 97%
rename from templates/zerver/home.html
rename to templates/zerver/app/home.html
index fbbf54f5a3..aa11d3ed22 100644
--- a/templates/zerver/home.html
+++ b/templates/zerver/app/home.html
@@ -131,8 +131,8 @@
 </div>
 
 
-{% include "zerver/message_history.html" %}
-{% include "zerver/delete_message.html" %}
-{% include "zerver/compose.html" %}
+{% include "zerver/app/message_history.html" %}
+{% include "zerver/app/delete_message.html" %}
+{% include "zerver/app/compose.html" %}
 <div id="notifications-area">
 </div>
diff --git a/templates/zerver/index.html b/templates/zerver/app/index.html
similarity index 87%
rename from templates/zerver/index.html
rename to templates/zerver/app/index.html
index 527d437e3d..1f0f65fa19 100644
--- a/templates/zerver/index.html
+++ b/templates/zerver/app/index.html
@@ -41,7 +41,7 @@
 
     {{ render_bundle('katex') }}
 
-    {% include "zerver/topic_is_muted.html" %}
+    {% include "zerver/app/topic_is_muted.html" %}
 
 {% endblock %}
 {% block content %}
@@ -59,14 +59,14 @@
     </script>
 </div>
 
-{% include "zerver/lightbox_overlay.html" %}
-{% include "zerver/subscriptions.html" %}
-{% include "zerver/drafts.html" %}
+{% include "zerver/app/lightbox_overlay.html" %}
+{% include "zerver/app/subscriptions.html" %}
+{% include "zerver/app/drafts.html" %}
 <div id="settings_overlay_container" class="overlay" data-overlay="settings" aria-hidden="true">
-    {% include "zerver/settings_overlay.html" %}
+    {% include "zerver/app/settings_overlay.html" %}
 </div>
 
-{% include "zerver/navbar.html" %}
+{% include "zerver/app/navbar.html" %}
 
 <div class="fixed-app">
     <div class="app-main">
@@ -105,7 +105,7 @@
     </div>
     <div class="app-main">
         <div class="column-left">
-            {% include "zerver/left_sidebar.html" %}
+            {% include "zerver/app/left_sidebar.html" %}
         </div>
         <div class="column-middle">
             <div class="column-middle-inner tab-content">
@@ -132,18 +132,18 @@
                             </div>
                         </div>
                     </div>
-                    {% include "zerver/home.html" %}
+                    {% include "zerver/app/home.html" %}
                 </div>
 
                 {% if show_debug %}
                 <div class="tab-pane" id="debug">
-                    {% include "zerver/debug.html" %}
+                    {% include "zerver/app/debug.html" %}
                 </div>
                 {% endif %}
             </div><!--/tab-content-->
         </div>
         <div class="column-right">
-            {% include "zerver/right_sidebar.html" %}
+            {% include "zerver/app/right_sidebar.html" %}
         </div><!--/right sidebar-->
     </div><!--/row-->
     <div class="informational-overlays overlay new-style" data-overlay="informationalOverlays" aria-hidden="true">
@@ -152,16 +152,16 @@
                 <button class="button no-style exit">&times;</button>
             </div>
             <div class="overlay-body">
-                {% include "zerver/keyboard_shortcuts.html" %}
-                {% include "zerver/search_operators.html" %}
-                {% include "zerver/markdown_help.html" %}
+                {% include "zerver/app/keyboard_shortcuts.html" %}
+                {% include "zerver/app/search_operators.html" %}
+                {% include "zerver/app/markdown_help.html" %}
             </div>
         </div>
     </div>
-    {% include "zerver/invite_user.html" %}
-    {% include "zerver/bankruptcy.html" %}
-    {% include "zerver/logout.html" %}
-    {% include "zerver/deprecation_notice.html" %}
+    {% include "zerver/app/invite_user.html" %}
+    {% include "zerver/app/bankruptcy.html" %}
+    {% include "zerver/app/logout.html" %}
+    {% include "zerver/app/deprecation_notice.html" %}
     <div class='notifications top-right'></div>
 </div>
 {% endblock %}
diff --git a/templates/zerver/invite_user.html b/templates/zerver/app/invite_user.html
similarity index 100%
rename from templates/zerver/invite_user.html
rename to templates/zerver/app/invite_user.html
diff --git a/templates/zerver/keyboard_shortcuts.html b/templates/zerver/app/keyboard_shortcuts.html
similarity index 100%
rename from templates/zerver/keyboard_shortcuts.html
rename to templates/zerver/app/keyboard_shortcuts.html
diff --git a/templates/zerver/left_sidebar.html b/templates/zerver/app/left_sidebar.html
similarity index 100%
rename from templates/zerver/left_sidebar.html
rename to templates/zerver/app/left_sidebar.html
diff --git a/templates/zerver/lightbox_overlay.html b/templates/zerver/app/lightbox_overlay.html
similarity index 100%
rename from templates/zerver/lightbox_overlay.html
rename to templates/zerver/app/lightbox_overlay.html
diff --git a/templates/zerver/logout.html b/templates/zerver/app/logout.html
similarity index 100%
rename from templates/zerver/logout.html
rename to templates/zerver/app/logout.html
diff --git a/templates/zerver/markdown_help.html b/templates/zerver/app/markdown_help.html
similarity index 100%
rename from templates/zerver/markdown_help.html
rename to templates/zerver/app/markdown_help.html
diff --git a/templates/zerver/message_history.html b/templates/zerver/app/message_history.html
similarity index 100%
rename from templates/zerver/message_history.html
rename to templates/zerver/app/message_history.html
diff --git a/templates/zerver/navbar.html b/templates/zerver/app/navbar.html
similarity index 100%
rename from templates/zerver/navbar.html
rename to templates/zerver/app/navbar.html
diff --git a/templates/zerver/right_sidebar.html b/templates/zerver/app/right_sidebar.html
similarity index 100%
rename from templates/zerver/right_sidebar.html
rename to templates/zerver/app/right_sidebar.html
diff --git a/templates/zerver/search_operators.html b/templates/zerver/app/search_operators.html
similarity index 100%
rename from templates/zerver/search_operators.html
rename to templates/zerver/app/search_operators.html
diff --git a/templates/zerver/settings_overlay.html b/templates/zerver/app/settings_overlay.html
similarity index 99%
rename from templates/zerver/settings_overlay.html
rename to templates/zerver/app/settings_overlay.html
index 2b3f0100c5..96ac3074af 100644
--- a/templates/zerver/settings_overlay.html
+++ b/templates/zerver/app/settings_overlay.html
@@ -136,6 +136,6 @@
             </div>
         </div>
 
-        {% include "zerver/settings_sidebar.html" %}
+        {% include "zerver/app/settings_sidebar.html" %}
     </div>
 </div>
diff --git a/templates/zerver/settings_sidebar.html b/templates/zerver/app/settings_sidebar.html
similarity index 100%
rename from templates/zerver/settings_sidebar.html
rename to templates/zerver/app/settings_sidebar.html
diff --git a/templates/zerver/subscriptions.html b/templates/zerver/app/subscriptions.html
similarity index 100%
rename from templates/zerver/subscriptions.html
rename to templates/zerver/app/subscriptions.html
diff --git a/templates/zerver/topic_is_muted.html b/templates/zerver/app/topic_is_muted.html
similarity index 100%
rename from templates/zerver/topic_is_muted.html
rename to templates/zerver/app/topic_is_muted.html
diff --git a/templates/zerver/portico-header-dropdown.html b/templates/zerver/portico-header-dropdown.html
index 87611d366d..10afa09d83 100644
--- a/templates/zerver/portico-header-dropdown.html
+++ b/templates/zerver/portico-header-dropdown.html
@@ -11,7 +11,7 @@
             </a>
         </li>
         <li>
-            {% include 'zerver/logout.html' %}
+            {% include 'zerver/app/logout.html' %}
             <a href="#logout">
                 <span class="logout">
                     <i class="icon-vector-off"></i>
diff --git a/tools/check-templates b/tools/check-templates
index 80756e7f91..e3ff742c33 100755
--- a/tools/check-templates
+++ b/tools/check-templates
@@ -100,7 +100,7 @@ def check_html_templates(templates, all_dups):
             # prevent cleaning them.
             'templates/corporate/zephyr-mirror.html',
             # Can't clean this because of `preserve_spaces`
-            'templates/zerver/markdown_help.html',
+            'templates/zerver/app/markdown_help.html',
         ]
         validate(fn=fn, check_indent=(fn not in bad_files))
 
@@ -111,7 +111,7 @@ def check_html_templates(templates, all_dups):
         # to convert it to a /help/ markdown article.
         'templates/corporate/zephyr-mirror.html',
         # Can't clean this because of `preserve_spaces`
-        'templates/zerver/markdown_help.html',
+        'templates/zerver/app/markdown_help.html',
     ]
     # TODO: Clean these files
     for fn in templates:
diff --git a/tools/linter_lib/custom_check.py b/tools/linter_lib/custom_check.py
index bffdb1e33d..3dff441520 100644
--- a/tools/linter_lib/custom_check.py
+++ b/tools/linter_lib/custom_check.py
@@ -614,7 +614,7 @@ def build_custom_checkers(by_lang):
          'bad_lines': ["<p title='foo'></p>"]},
         {'pattern': 'title="[^{\:]',
          'exclude_line': set([
-             ('templates/zerver/markdown_help.html',
+             ('templates/zerver/app/markdown_help.html',
               '<td><img alt=":heart:" class="emoji" src="/static/generated/emoji/images/emoji/heart.png" title=":heart:" /></td>')
          ]),
          'exclude': set(["templates/zerver/emails"]),
@@ -622,8 +622,8 @@ def build_custom_checkers(by_lang):
         {'pattern': '\Walt=["\'][^{"\']',
          'description': "alt argument should be enclosed by _() or it should be an empty string.",
          'exclude': set(['static/templates/settings/display-settings.handlebars',
-                         'templates/zerver/keyboard_shortcuts.html',
-                         'templates/zerver/markdown_help.html']),
+                         'templates/zerver/app/keyboard_shortcuts.html',
+                         'templates/zerver/app/markdown_help.html']),
          'good_lines': ['<img src="{{source_url}}" alt="{{ _(name) }}" />', '<img alg="" />'],
          'bad_lines': ['<img alt="Foo Image" />']},
         {'pattern': '\Walt=["\']{{ ?["\']',
@@ -642,7 +642,7 @@ def build_custom_checkers(by_lang):
          'exclude_pattern': r'.*style ?=["' + "'" + '](display: ?none|background: {{|color: {{|background-color: {{).*',
          'exclude': set([
              # KaTeX output uses style attribute
-             'templates/zerver/markdown_help.html',
+             'templates/zerver/app/markdown_help.html',
              # 5xx page doesn't have external CSS
              'static/html/5xx.html',
              # Group PMs color is dynamically calculated
@@ -665,14 +665,14 @@ def build_custom_checkers(by_lang):
              'templates/zerver/email_log.html',
 
              # Probably just needs to be changed to display: none so the exclude works
-             'templates/zerver/navbar.html',
+             'templates/zerver/app/navbar.html',
 
              # Needs the width cleaned up; display: none is fine
              'static/templates/settings/account-settings.handlebars',
 
              # Inline styling for an svg; could be moved to CSS files?
              'templates/zerver/landing_nav.html',
-             'templates/zerver/home.html',
+             'templates/zerver/app/home.html',
              'templates/zerver/features.html',
              'templates/zerver/portico-header.html',
 
diff --git a/zerver/views/home.py b/zerver/views/home.py
index 3367d7b0b5..ca39fafd02 100644
--- a/zerver/views/home.py
+++ b/zerver/views/home.py
@@ -236,7 +236,7 @@ def home_real(request: HttpRequest) -> HttpResponse:
         show_invites = False
 
     request._log_data['extra'] = "[%s]" % (register_ret["queue_id"],)
-    response = render(request, 'zerver/index.html',
+    response = render(request, 'zerver/app/index.html',
                       context={'user_profile': user_profile,
                                'page_params': JSONEncoderForHTML().encode(page_params),
                                'nofontface': is_buggy_ua(request.META.get("HTTP_USER_AGENT", "Unspecified")),