diff --git a/swh/web/api/apiurls.py b/swh/web/api/apiurls.py
--- a/swh/web/api/apiurls.py
+++ b/swh/web/api/apiurls.py
@@ -83,7 +83,7 @@
 
     """
 
-    url_pattern = "^" + api_version + url_pattern + "$"
+    url_pattern = "^api/" + api_version + url_pattern + "$"
 
     def decorator(f):
         # create a DRF view from the wrapped function
diff --git a/swh/web/api/views/utils.py b/swh/web/api/views/utils.py
--- a/swh/web/api/views/utils.py
+++ b/swh/web/api/views/utils.py
@@ -77,7 +77,7 @@
     return Response({}, template_name="api/api.html")
 
 
-APIUrls.add_url_pattern(r"^$", api_home, view_name="api-1-homepage")
+APIUrls.add_url_pattern(r"^api/$", api_home, view_name="api-1-homepage")
 
 
 @api_route(r"/", "api-1-endpoints")
diff --git a/swh/web/browse/browseurls.py b/swh/web/browse/browseurls.py
--- a/swh/web/browse/browseurls.py
+++ b/swh/web/browse/browseurls.py
@@ -30,7 +30,7 @@
         view_name: the name of the Django view associated to the routes used
             to reverse the url
     """
-    url_patterns = tuple("^" + url_pattern + "$" for url_pattern in url_patterns)
+    url_patterns = tuple("^browse/" + url_pattern + "$" for url_pattern in url_patterns)
     view_name = view_name
 
     def decorator(f):
diff --git a/swh/web/browse/urls.py b/swh/web/browse/urls.py
--- a/swh/web/browse/urls.py
+++ b/swh/web/browse/urls.py
@@ -48,16 +48,16 @@
 
 
 urlpatterns = [
-    url(r"^$", _browse_search_view),
-    url(r"^help/$", _browse_help_view, name="browse-help"),
-    url(r"^search/$", _browse_search_view, name="browse-search"),
-    url(r"^vault/$", _browse_vault_view, name="browse-vault"),
+    url(r"^browse/$", _browse_search_view),
+    url(r"^browse/help/$", _browse_help_view, name="browse-help"),
+    url(r"^browse/search/$", _browse_search_view, name="browse-search"),
+    url(r"^browse/vault/$", _browse_vault_view, name="browse-vault"),
     # for backward compatibility
-    url(r"^origin/save/$", _browse_origin_save_view, name="browse-origin-save"),
+    url(r"^browse/origin/save/$", _browse_origin_save_view, name="browse-origin-save"),
     url(
-        r"^(?P<swhid>swh:[0-9]+:[a-z]+:[0-9a-f]+.*)/$",
+        r"^browse/(?P<swhid>swh:[0-9]+:[a-z]+:[0-9a-f]+.*)/$",
         swhid_browse,
-        name="browse-swhid",
+        name="browse-swhid-legacy",
     ),
 ]
 
diff --git a/swh/web/common/utils.py b/swh/web/common/utils.py
--- a/swh/web/common/utils.py
+++ b/swh/web/common/utils.py
@@ -21,6 +21,7 @@
 import requests
 from requests.auth import HTTPBasicAuth
 
+from django.conf import settings
 from django.core.cache import cache
 from django.core.cache.backends.base import DEFAULT_TIMEOUT
 from django.http import HttpRequest, QueryDict
@@ -40,6 +41,7 @@
 
 SWHID_RE = "swh:1:[a-z]{3}:[0-9a-z]{40}"
 
+
 swh_object_icons = {
     "alias": "mdi mdi-star",
     "branch": "mdi mdi-source-branch",
@@ -320,6 +322,7 @@
         "MAILMAP_ADMIN_PERMISSION": MAILMAP_ADMIN_PERMISSION,
         "lang": "en",
         "sidebar_state": request.COOKIES.get("sidebar-state", "expanded"),
+        "SWH_DJANGO_APPS": settings.SWH_DJANGO_APPS,
     }
 
 
diff --git a/swh/web/config.py b/swh/web/config.py
--- a/swh/web/config.py
+++ b/swh/web/config.py
@@ -1,4 +1,4 @@
-# Copyright (C) 2017-2021  The Software Heritage developers
+# Copyright (C) 2017-2022  The Software Heritage developers
 # See the AUTHORS file at the top-level directory of this distribution
 # License: GNU Affero General Public License version 3, or any later version
 # See top-level LICENSE file for more information
@@ -155,6 +155,13 @@
     "give": ("dict", {"public_key": "", "token": ""}),
     "features": ("dict", {"add_forge_now": True}),
     "add_forge_now": ("dict", {"email_address": "add-forge-now@example.com"}),
+    "swh_extra_django_apps": (
+        "list",
+        [
+            "swh.web.inbound_email",
+            "swh.web.add_forge_now",
+        ],
+    ),
 }
 
 swhweb_config: Dict[str, Any] = {}
diff --git a/swh/web/settings/common.py b/swh/web/settings/common.py
--- a/swh/web/settings/common.py
+++ b/swh/web/settings/common.py
@@ -8,6 +8,7 @@
 Django common settings for swh-web.
 """
 
+from importlib.util import find_spec
 import os
 import sys
 from typing import Any, Dict
@@ -42,6 +43,21 @@
 
 # Application definition
 
+SWH_BASE_DJANGO_APPS = [
+    "swh.web.auth",
+    "swh.web.browse",
+    "swh.web.common",
+    "swh.web.api",
+]
+SWH_EXTRA_DJANGO_APPS = [
+    app
+    for app in swh_web_config["swh_extra_django_apps"]
+    if app not in SWH_BASE_DJANGO_APPS
+]
+# swh.web.api must be the last loaded application due to the way
+# its URLS are registered
+SWH_DJANGO_APPS = SWH_EXTRA_DJANGO_APPS + SWH_BASE_DJANGO_APPS
+
 INSTALLED_APPS = [
     "django.contrib.admin",
     "django.contrib.auth",
@@ -50,16 +66,10 @@
     "django.contrib.messages",
     "django.contrib.staticfiles",
     "rest_framework",
-    "swh.web.common",
-    "swh.web.inbound_email",
-    "swh.web.api",
-    "swh.web.auth",
-    "swh.web.browse",
-    "swh.web.add_forge_now",
     "webpack_loader",
     "django_js_reverse",
     "corsheaders",
-]
+] + SWH_DJANGO_APPS
 
 MIDDLEWARE = [
     "django.middleware.security.SecurityMiddleware",
@@ -84,10 +94,23 @@
 
 ROOT_URLCONF = "swh.web.urls"
 
+SWH_APP_TEMPLATES = [os.path.join(PROJECT_DIR, "../templates")]
+# Add templates directory from each SWH Django application
+for app in SWH_DJANGO_APPS:
+    try:
+        app_spec = find_spec(app)
+        assert app_spec is not None, f"Django application {app} not found !"
+        assert app_spec.origin is not None
+        SWH_APP_TEMPLATES.append(
+            os.path.join(os.path.dirname(app_spec.origin), "templates")
+        )
+    except ModuleNotFoundError:
+        assert False, f"Django application {app} not found !"
+
 TEMPLATES = [
     {
         "BACKEND": "django.template.backends.django.DjangoTemplates",
-        "DIRS": [os.path.join(PROJECT_DIR, "../templates")],
+        "DIRS": SWH_APP_TEMPLATES,
         "APP_DIRS": True,
         "OPTIONS": {
             "context_processors": [
diff --git a/swh/web/tests/conftest.py b/swh/web/tests/conftest.py
--- a/swh/web/tests/conftest.py
+++ b/swh/web/tests/conftest.py
@@ -6,6 +6,7 @@
 from collections import defaultdict
 from datetime import timedelta
 import functools
+from importlib import import_module, reload
 import json
 import os
 import random
@@ -17,10 +18,12 @@
 from _pytest.python import Function
 from hypothesis import HealthCheck, settings
 import pytest
+from pytest_django.fixtures import SettingsWrapper
 
 from django.contrib.auth.models import User
 from django.core.cache import cache
 from django.test.utils import setup_databases
+from django.urls import clear_url_caches
 from rest_framework.test import APIClient, APIRequestFactory
 
 from swh.model.hashutil import (
@@ -1202,3 +1205,35 @@
     mailmap_user = User.objects.create_user(username="mailmap-user", password="")
     mailmap_user.user_permissions.add(create_django_permission(MAILMAP_PERMISSION))
     return mailmap_user
+
+
+def reload_urlconf():
+    from django.conf import settings
+
+    clear_url_caches()
+    urlconf = settings.ROOT_URLCONF
+    if urlconf in sys.modules:
+        reload(sys.modules[urlconf])
+    else:
+        import_module(urlconf)
+
+
+class SwhSettingsWrapper(SettingsWrapper):
+    def __setattr__(self, attr: str, value) -> None:
+        super().__setattr__(attr, value)
+        reload_urlconf()
+
+    def finalize(self) -> None:
+        super().finalize()
+        reload_urlconf()
+
+
+@pytest.fixture
+def django_settings():
+    """Override pytest-django settings fixture in order to reload URLs
+    when modifying settings in test and after test execution as most of
+    them depend on installed django apps in swh-web.
+    """
+    settings = SwhSettingsWrapper()
+    yield settings
+    settings.finalize()
diff --git a/swh/web/tests/test_urls.py b/swh/web/tests/test_urls.py
--- a/swh/web/tests/test_urls.py
+++ b/swh/web/tests/test_urls.py
@@ -3,11 +3,25 @@
 # License: GNU Affero General Public License version 3, or any later version
 # See top-level LICENSE file for more information
 
+import pytest
+
 from django.urls import get_resolver
 
 
 def test_swh_web_urls_have_trailing_slash():
-    urls = set(value[1] for value in get_resolver().reverse_dict.values())
+    urls = set(
+        value[1]
+        for key, value in get_resolver().reverse_dict.items()
+        if key != "browse-swhid"  # (see T3234)
+    )
     for url in urls:
         if url != "$":
             assert url.endswith("/$")
+
+
+def test_urls_registration_error_for_not_found_django_app(django_settings):
+    app_name = "swh.web.foobar"
+    with pytest.raises(
+        AssertionError, match=f"Django application {app_name} not found !"
+    ):
+        django_settings.SWH_DJANGO_APPS = django_settings.SWH_DJANGO_APPS + [app_name]
diff --git a/swh/web/urls.py b/swh/web/urls.py
--- a/swh/web/urls.py
+++ b/swh/web/urls.py
@@ -3,6 +3,7 @@
 # License: GNU Affero General Public License version 3, or any later version
 # See top-level LICENSE file for more information
 
+from importlib.util import find_spec
 
 from django_js_reverse.views import urls_js
 
@@ -38,8 +39,6 @@
 urlpatterns = [
     url(r"^admin/", include("swh.web.admin.urls")),
     url(r"^favicon\.ico/$", favicon_view),
-    url(r"^api/", include("swh.web.api.urls")),
-    url(r"^browse/", include("swh.web.browse.urls")),
     url(r"^$", _default_view, name="swh-web-homepage"),
     url(r"^jsreverse/$", urls_js, name="js_reverse"),
     # keep legacy SWHID resolving URL with trailing slash for backward compatibility
@@ -58,6 +57,16 @@
     url(r"^logout/$", LogoutView.as_view(template_name="logout.html"), name="logout"),
 ]
 
+# Register URLs for each SWH Django application
+for app in settings.SWH_DJANGO_APPS:
+    app_urls = app + ".urls"
+    try:
+        app_urls_spec = find_spec(app_urls)
+        if app_urls_spec is not None:
+            urlpatterns.append(url(r"^", include(app_urls)))
+    except ModuleNotFoundError:
+        assert False, f"Django application {app} not found !"
+
 if is_feature_enabled("add_forge_now"):
     urlpatterns += (url(r"^", include("swh.web.add_forge_now.views")),)