diff --git a/Dockerfile b/Dockerfile
index 3295f7d728e1..a1e58b08ab26 100644
--- a/Dockerfile
+++ b/Dockerfile
@@ -91,6 +91,11 @@ rm -rf /deps/build/*
 ${PIP_COMMAND} install --progress-bar=off --no-deps --exists-action=w -r requirements/pip.txt
 EOF
 
+# Expose the DOCKER_TARGET variable to all subsequent stages
+# This value is used to determine if we are building for production or development
+ARG DOCKER_TARGET
+ENV DOCKER_TARGET=${DOCKER_TARGET}
+
 # Define production dependencies as a single layer
 # let's the rest of the stages inherit prod dependencies
 # and makes copying the /deps dir to the final layer easy.
diff --git a/Makefile-docker b/Makefile-docker
index 0c870b1aea73..05d87b8fcf85 100644
--- a/Makefile-docker
+++ b/Makefile-docker
@@ -28,7 +28,12 @@ check_debian_packages: ## check the existence of multiple debian packages
 
 .PHONY: check_pip_packages
 check_pip_packages: ## check the existence of multiple python packages
-	./scripts/check_pip_packages.sh prod.txt dev.txt
+	@ ./scripts/check_pip_packages.sh prod.txt
+# "production" corresponds to the "propduction" DOCKER_TARGET defined in the Dockerfile
+# When the target is "production" it means we cannot expect dev.txt dependencies to be installed.
+	@if [ "$(DOCKER_TARGET)" != "production" ]; then \
+		./scripts/check_pip_packages.sh dev.txt; \
+	fi
 
 .PHONY: check_files
 check_files: ## check the existence of multiple files
diff --git a/docker-bake.hcl b/docker-bake.hcl
index 0499483bd653..746b9034c88e 100644
--- a/docker-bake.hcl
+++ b/docker-bake.hcl
@@ -18,6 +18,7 @@ target "web" {
 	DOCKER_COMMIT = "${DOCKER_COMMIT}"
 	DOCKER_VERSION = "${DOCKER_VERSION}"
 	DOCKER_BUILD = "${DOCKER_BUILD}"
+  DOCKER_TARGET = "${DOCKER_TARGET}"
   }
   pull = true
 
diff --git a/docker-compose.ci.yml b/docker-compose.ci.yml
index d45eebd5db3f..72863e437745 100644
--- a/docker-compose.ci.yml
+++ b/docker-compose.ci.yml
@@ -2,20 +2,12 @@ services:
   worker:
     environment:
       - HOST_UID=9500
-      - DEBUG=
     volumes:
       - /data/olympia
 
   web:
     extends:
       service: worker
-    volumes:
-      - data_site_static:/data/olympia/site-static
-
-  nginx:
-    volumes:
-      - data_site_static:/srv/site-static
 
 volumes:
   data_olympia:
-  data_site_static:
diff --git a/docker-compose.yml b/docker-compose.yml
index 196ad8c143f3..27eb9eca3eff 100644
--- a/docker-compose.yml
+++ b/docker-compose.yml
@@ -39,7 +39,7 @@ x-olympia: &olympia
   entrypoint: ["/data/olympia/docker/entrypoint.sh"]
 
 services:
-  worker: &worker
+  worker:
     <<: *olympia
     command: [
       "DJANGO_SETTINGS_MODULE=settings",
@@ -84,7 +84,8 @@ services:
       - autograph
 
   web:
-    <<: *worker
+    extends:
+      service: worker
     healthcheck:
       test: ["CMD-SHELL", "curl --fail --show-error --include --location http://127.0.0.1:8002/__version__"]
       retries: 3
@@ -98,7 +99,7 @@ services:
     image: nginx
     volumes:
       - ./docker/nginx/addons.conf:/etc/nginx/conf.d/addons.conf
-      - ./static:/srv/site-static
+      - ./static:/srv/static
       - storage:/srv/user-media
     ports:
       - "80:80"
diff --git a/docker/nginx/addons.conf b/docker/nginx/addons.conf
index 1d87ec43acc7..3948258aa410 100644
--- a/docker/nginx/addons.conf
+++ b/docker/nginx/addons.conf
@@ -11,7 +11,7 @@ server {
     }
 
     location /static/ {
-         alias /srv/site-static/;
+         alias /srv/static/;
 
          # Fallback to the uwsgi server if the file is not found in the static files directory.
          # This will happen for vendor files from pytnon or npm dependencies that won't be available
diff --git a/docs/topics/development/static-files.md b/docs/topics/development/static-files.md
index 768d237f77db..46a4e3ffc377 100644
--- a/docs/topics/development/static-files.md
+++ b/docs/topics/development/static-files.md
@@ -1,6 +1,7 @@
 # Static Files in addons-server
 
-This document explains how static files are served in the addons-server project during local development.
+This document explains how static files are served in the addons-server project during local development. In production,
+static files are served directly from a CDN.
 
 ## Overview
 
@@ -10,6 +11,7 @@ These files come from multiple sources:
 1. The `./static` folder in the project
 2. Python dependencies
 3. npm dependencies
+4. Compressed/minified files built by `update_assets`
 
 ## Static File Servers
 
@@ -29,6 +31,30 @@ The `web` container exposes the `site-static` directory to nginx that includes t
 
 ## Static File Sources
 
+The rendering path for static files is as follows:
+
+1. Nginx tries to serve the file if it is available in the `./static` directory.
+2. If the file is not found, the request is forwarded to django and served by the static file server.
+
+The static file serve uses our defined `STATICFILES_STORAGE` setting to determine the URL for static files as well as their underlying source file.
+During development, we use the `StaticFilesStorage` class which does not map the hashed file names back to their original file names.
+Otherwise we use the same `ManifestStaticFilesStorage` class that is used in production, expecting to serve the files from the `STATIC_ROOT` directory.
+
+This allows us to skip `update_assets` in dev mode, speeding up the development process, while still enabling production-like behavior
+when configured to do so. The long term goal is to run CI in production mode always to ensure all tests verify against the production
+static file build.
+
+To better visualize the impact of the various settings, here is a reference:
+
+Given a static file 'js/devhub/my-file.js':
+
+In `DEV_MODE` the url will look like `/static/js/devhub/my-file.js` no matter what.
+However, in production, if `DEBUG` is `False`, the url will append the content hash like this,
+`/static/js/devhub/my-file.1234567890.js`. Finally, if `DEBUG` is true, this file will be minified and concatenated with other files and probably look something like this `/static/js/devhub-all.min.1234567890.js`.
+
+The true `production` mode is then when `DEBUG` is `False` and `DEV_MODE` is `False`. But it makes sense
+to make these individually toggleable so you can better "debug" js files from a production image.
+
 ### Project Static Files
 
 Static files specific to the addons-server project are stored in the `./static` directory. These include CSS, JavaScript, images, and other assets used by the application.
@@ -59,23 +85,3 @@ During development they are served by the django development server.
 
 We have a (complex) set of npm static assets that are built by the `compress_assets` management command.
 During development, these assets are served directly from the node_modules directory using a custom static finder.
-
-## DEBUG Property and Static File Serving
-
-The behavior of static file serving can be controlled using the `DEBUG` environment variable or via setting it directly in
-the `local_settings.py` file. Be careful directly setting this value, if DEBUG is set to false, and you don't have sufficient
-routing setup to serve files fron nginx only, it can cause failure to serve some static files.
-
-It is best to use  the compose file to control DEBUG.a
-
-This is set in the environment, and in CI environments, it's controlled by the `docker-compose.ci.yml` file.
-
-The `DEBUG` property is what is used by django to determine if it should serve static files or not. In development,
-you can manually override this in the make up command, but in general, you should rely on the `docker-compose.ci.yml` file
-to set the correct value as this will also set appropriate file mounts.
-
-```bash
-make up COMPOSE_FILE=docker-compose.yml:docker-compose.ci.yml
-```
-
-This will run addons-server in production mode, serving files from the `site-static` directory.
diff --git a/docs/topics/development/troubleshooting_and_debugging.md b/docs/topics/development/troubleshooting_and_debugging.md
index b00e92482be3..86443cef935f 100644
--- a/docs/topics/development/troubleshooting_and_debugging.md
+++ b/docs/topics/development/troubleshooting_and_debugging.md
@@ -2,6 +2,22 @@
 
 Effective troubleshooting and debugging practices are essential for maintaining and improving the **addons-server** project. This section covers common issues, their solutions, and tools for effective debugging.
 
+## DEV_MODE vs DEBUG
+
+In our project, `DEV_MODE` and `DEBUG` serve distinct but complementary purposes.
+`DEV_MODE` is directly tied to the `DOCKER_TARGET` environment variable and is used to enable or disable behaviors
+based on whether we are running a production image or not.
+
+For instance, production images always disables certain features like using fake fxa authentication. Additionally,
+certain dependencies are only installed in [dev.txt](../../../requirements/dev.txt) and so must be disabled in production.
+
+Conversely, `DEBUG` controls the activation of debugging tools and utilities, such as the debug_toolbar,
+which are useful for troubleshooting. Unlike DEV_MODE, DEBUG is independent
+and can be toggled in both development and production environments as needed.
+
+This separation ensures that essential behaviors are managed according to the deployment target (DEV_MODE),
+while allowing flexibility to enable or disable debugging features (DEBUG) in production or development images.
+
 ## Common Issues and Solutions
 
 1. **Containers Not Starting**:
diff --git a/settings.py b/settings.py
index 0c38f88a4c07..c8ee47249f56 100644
--- a/settings.py
+++ b/settings.py
@@ -12,15 +12,21 @@
 from olympia.lib.settings_base import *  # noqa
 
 
+# "production" is a named docker stage corresponding to the production image.
+# when we build the production image, the stage to use is determined
+# via the "DOCKER_TARGET" variable which is also passed into the image.
+# So if the value is anything other than "production" we are in development mode.
+DEV_MODE = DOCKER_TARGET != 'production'
+
 WSGI_APPLICATION = 'olympia.wsgi.application'
 
 INTERNAL_ROUTES_ALLOWED = True
 
+# Always
+SERVE_STATIC_FILES = True
+
 # These apps are great during development.
-INSTALLED_APPS += (
-    'olympia.landfill',
-    'dbbackup',
-)
+INSTALLED_APPS += ('olympia.landfill',)
 
 DBBACKUP_STORAGE = 'django.core.files.storage.FileSystemStorage'
 
@@ -53,8 +59,11 @@ def insert_debug_toolbar_middleware(middlewares):
     return tuple(ret_middleware)
 
 
-if DEBUG:
-    INSTALLED_APPS += ('debug_toolbar',)
+if DEV_MODE:
+    INSTALLED_APPS += (
+        'debug_toolbar',
+        'dbbackup',
+    )
     MIDDLEWARE = insert_debug_toolbar_middleware(MIDDLEWARE)
 
 DEBUG_TOOLBAR_CONFIG = {
@@ -107,7 +116,7 @@ def insert_debug_toolbar_middleware(middlewares):
 FXA_OAUTH_HOST = 'https://oauth.stage.mozaws.net/v1'
 FXA_PROFILE_HOST = 'https://profile.stage.mozaws.net/v1'
 
-# When USE_FAKE_FXA_AUTH and settings.DEBUG are both True, we serve a fake
+# When USE_FAKE_FXA_AUTH and settings.DEV_MODE are both True, we serve a fake
 # authentication page, bypassing FxA. To disable this behavior, set
 # USE_FAKE_FXA = False in your local settings.
 # You will also need to specify `client_id` and `client_secret` in your
diff --git a/settings_test.py b/settings_test.py
index 883c636807ca..f6912f35a882 100644
--- a/settings_test.py
+++ b/settings_test.py
@@ -23,6 +23,8 @@
 IN_TEST_SUITE = True
 
 DEBUG = False
+# We should default to production mode unless otherwise specified
+DEV_MODE = False
 
 # We won't actually send an email.
 SEND_REAL_EMAIL = True
diff --git a/src/olympia/accounts/tests/test_utils.py b/src/olympia/accounts/tests/test_utils.py
index df3d0f258b54..6f92c123636f 100644
--- a/src/olympia/accounts/tests/test_utils.py
+++ b/src/olympia/accounts/tests/test_utils.py
@@ -292,7 +292,7 @@ def test_redirect_for_login_with_2fa_enforced_and_config():
     assert request.session['enforce_2fa'] is True
 
 
-@override_settings(DEBUG=True, USE_FAKE_FXA_AUTH=True)
+@override_settings(DEV_MODE=True, USE_FAKE_FXA_AUTH=True)
 def test_fxa_login_url_when_faking_fxa_auth():
     path = '/en-US/addons/abp/?source=ddg'
     request = RequestFactory().get(path)
diff --git a/src/olympia/accounts/tests/test_verify.py b/src/olympia/accounts/tests/test_verify.py
index 9da8928de21b..0b0af2129933 100644
--- a/src/olympia/accounts/tests/test_verify.py
+++ b/src/olympia/accounts/tests/test_verify.py
@@ -234,7 +234,7 @@ def test_with_id_token(self):
         self.get_profile.assert_called_with('cafe')
 
 
-@override_settings(USE_FAKE_FXA_AUTH=False, DEBUG=True, VERIFY_FXA_ACCESS_TOKEN=True)
+@override_settings(USE_FAKE_FXA_AUTH=False, DEV_MODE=True, VERIFY_FXA_ACCESS_TOKEN=True)
 class TestCheckAndUpdateFxaAccessToken(TestCase):
     def setUp(self):
         super().setUp()
diff --git a/src/olympia/accounts/tests/test_views.py b/src/olympia/accounts/tests/test_views.py
index b3e6d3027037..4b0f285bb74e 100644
--- a/src/olympia/accounts/tests/test_views.py
+++ b/src/olympia/accounts/tests/test_views.py
@@ -172,7 +172,7 @@ def has_cors_headers(response, origin='https://addons-frontend'):
 
 
 class TestLoginStartView(TestCase):
-    @override_settings(DEBUG=True, USE_FAKE_FXA_AUTH=True)
+    @override_settings(DEV_MODE=True, USE_FAKE_FXA_AUTH=True)
     def test_redirect_url_fake_fxa_auth(self):
         response = self.client.get(reverse_ns('accounts.login_start'))
         assert response.status_code == 302
@@ -700,7 +700,7 @@ def test_waffle_flag_off_enforced_2fa_should_have_no_effect(self):
         self.request.session['enforce_2fa'] = True
         self._test_should_continue_without_redirect_for_two_factor_auth()
 
-    @override_settings(DEBUG=True, USE_FAKE_FXA_AUTH=True)
+    @override_settings(DEV_MODE=True, USE_FAKE_FXA_AUTH=True)
     def test_fake_fxa_auth(self):
         self.user = user_factory()
         self.find_user.return_value = self.user
@@ -721,7 +721,7 @@ def test_fake_fxa_auth(self):
         assert kwargs['next_path'] == '/a/path/?'
         assert self.fxa_identify.call_count == 0
 
-    @override_settings(DEBUG=True, USE_FAKE_FXA_AUTH=True)
+    @override_settings(DEV_MODE=True, USE_FAKE_FXA_AUTH=True)
     def test_fake_fxa_auth_with_2fa(self):
         self.user = user_factory()
         self.find_user.return_value = self.user
diff --git a/src/olympia/amo/tests/test_views.py b/src/olympia/amo/tests/test_views.py
index 2fff1e28ee69..7f8b54571f55 100644
--- a/src/olympia/amo/tests/test_views.py
+++ b/src/olympia/amo/tests/test_views.py
@@ -510,7 +510,7 @@ def test_allow_mozilla_collections(self):
 
 @pytest.mark.django_db
 def test_fake_fxa_authorization_correct_values_passed():
-    with override_settings(DEBUG=True):  # USE_FAKE_FXA_AUTH is already True
+    with override_settings(DEV_MODE=True):  # USE_FAKE_FXA_AUTH is already True
         url = reverse('fake-fxa-authorization')
         response = test.Client().get(url, {'state': 'foobar'})
         assert response.status_code == 200
@@ -528,15 +528,15 @@ def test_fake_fxa_authorization_correct_values_passed():
 @pytest.mark.django_db
 def test_fake_fxa_authorization_deactivated():
     url = reverse('fake-fxa-authorization')
-    with override_settings(DEBUG=False, USE_FAKE_FXA_AUTH=False):
+    with override_settings(DEV_MODE=False, USE_FAKE_FXA_AUTH=False):
         response = test.Client().get(url)
     assert response.status_code == 404
 
-    with override_settings(DEBUG=False, USE_FAKE_FXA_AUTH=True):
+    with override_settings(DEV_MODE=False, USE_FAKE_FXA_AUTH=True):
         response = test.Client().get(url)
     assert response.status_code == 404
 
-    with override_settings(DEBUG=True, USE_FAKE_FXA_AUTH=False):
+    with override_settings(DEV_MODE=True, USE_FAKE_FXA_AUTH=False):
         response = test.Client().get(url)
     assert response.status_code == 404
 
diff --git a/src/olympia/amo/utils.py b/src/olympia/amo/utils.py
index 78e248e3ba36..3ddd68a969cc 100644
--- a/src/olympia/amo/utils.py
+++ b/src/olympia/amo/utils.py
@@ -1165,7 +1165,7 @@ def extract_colors_from_image(path):
 def use_fake_fxa():
     """Return whether or not to use a fake FxA server for authentication.
     Should always return False in production"""
-    return settings.DEBUG and settings.USE_FAKE_FXA_AUTH
+    return settings.DEV_MODE and settings.USE_FAKE_FXA_AUTH
 
 
 class AMOJSONEncoder(JSONEncoder):
diff --git a/src/olympia/api/urls.py b/src/olympia/api/urls.py
index d0bbe8b47f99..7ff96027ade7 100644
--- a/src/olympia/api/urls.py
+++ b/src/olympia/api/urls.py
@@ -27,7 +27,7 @@ def get_versioned_api_routes(version, url_patterns):
     routes = url_patterns
 
     # For now, this feature is only enabled in dev mode
-    if settings.DEBUG:
+    if settings.DEV_MODE:
         routes.extend(
             [
                 re_path(
diff --git a/src/olympia/core/apps.py b/src/olympia/core/apps.py
index 6bc556df83ee..62d4264319bf 100644
--- a/src/olympia/core/apps.py
+++ b/src/olympia/core/apps.py
@@ -63,6 +63,9 @@ def static_check(app_configs, **kwargs):
     errors = []
     output = StringIO()
 
+    if settings.DEV_MODE:
+        return []
+
     try:
         call_command('compress_assets', dry_run=True, stdout=output)
         file_paths = output.getvalue().strip().split('\n')
diff --git a/src/olympia/devhub/templates/devhub/index.html b/src/olympia/devhub/templates/devhub/index.html
index de6195a10773..115dd23750f6 100644
--- a/src/olympia/devhub/templates/devhub/index.html
+++ b/src/olympia/devhub/templates/devhub/index.html
@@ -34,7 +34,7 @@
       <meta name="csrf" content="{{ csrf_token }}">
     {% endif %}
 
-    {% if settings.DEBUG %}
+    {% if settings.DEV_MODE %}
       {% if settings.LESS_LIVE_REFRESH %}
         <meta id="live_refresh" name="live_refresh" value="1">
       {% endif %}
diff --git a/src/olympia/landfill/management/commands/fetch_prod_addons.py b/src/olympia/landfill/management/commands/fetch_prod_addons.py
index 57a2608aa257..8bd59cd0c9b2 100644
--- a/src/olympia/landfill/management/commands/fetch_prod_addons.py
+++ b/src/olympia/landfill/management/commands/fetch_prod_addons.py
@@ -43,9 +43,9 @@ def add_arguments(self, parser):
         )
 
     def handle(self, *args, **options):
-        if not settings.DEBUG:
+        if not settings.DEV_MODE:
             raise CommandError(
-                'As a safety precaution this command only works if DEBUG=True.'
+                'As a safety precaution this command only works in DEV_MODE.'
             )
         self.fetch_addon_data(options)
 
diff --git a/src/olympia/landfill/management/commands/fetch_prod_versions.py b/src/olympia/landfill/management/commands/fetch_prod_versions.py
index 44167fe5d9e4..61df3c8ef964 100644
--- a/src/olympia/landfill/management/commands/fetch_prod_versions.py
+++ b/src/olympia/landfill/management/commands/fetch_prod_versions.py
@@ -28,9 +28,9 @@ def add_arguments(self, parser):
         )
 
     def handle(self, *args, **options):
-        if not settings.DEBUG:
+        if not settings.DEV_MODE:
             raise CommandError(
-                'As a safety precaution this command only works if DEBUG=True.'
+                'As a safety precaution this command only works in DEV_MODE.'
             )
         self.options = options
         self.fetch_versions_data()
diff --git a/src/olympia/landfill/management/commands/generate_addons.py b/src/olympia/landfill/management/commands/generate_addons.py
index 484a76d1f8fe..78889a83babe 100644
--- a/src/olympia/landfill/management/commands/generate_addons.py
+++ b/src/olympia/landfill/management/commands/generate_addons.py
@@ -46,10 +46,8 @@ def add_arguments(self, parser):
         )
 
     def handle(self, *args, **kwargs):
-        if not settings.DEBUG:
-            raise CommandError(
-                'You can only run this command with your DEBUG setting set to True.'
-            )
+        if not settings.DEV_MODE:
+            raise CommandError('You can only run this command in DEV_MODE.')
 
         num = int(kwargs.get('num'))
         email = kwargs.get('email')
diff --git a/src/olympia/landfill/management/commands/generate_themes.py b/src/olympia/landfill/management/commands/generate_themes.py
index 2775458e7efe..2f3f6da40c7f 100644
--- a/src/olympia/landfill/management/commands/generate_themes.py
+++ b/src/olympia/landfill/management/commands/generate_themes.py
@@ -37,10 +37,8 @@ def add_arguments(self, parser):
         )
 
     def handle(self, *args, **kwargs):
-        if not settings.DEBUG:
-            raise CommandError(
-                'You can only run this command with your DEBUG setting set to True.'
-            )
+        if not settings.DEV_MODE:
+            raise CommandError('You can only run this command in DEV_MODE.')
         num = int(kwargs.get('num'))
         email = kwargs.get('email')
 
diff --git a/src/olympia/lib/jingo_minify_helpers.py b/src/olympia/lib/jingo_minify_helpers.py
index ecc07f431761..e27bba689f09 100644
--- a/src/olympia/lib/jingo_minify_helpers.py
+++ b/src/olympia/lib/jingo_minify_helpers.py
@@ -38,10 +38,7 @@ def get_js_urls(bundle, debug=None):
         If True, return URLs for individual files instead of the minified
         bundle.
     """
-    if debug is None:
-        debug = settings.DEBUG
-
-    if debug:
+    if debug or settings.DEBUG or settings.DEV_MODE:
         return [static(item) for item in settings.MINIFY_BUNDLES['js'][bundle]]
     else:
         return [static(f'js/{bundle}-min.js')]
@@ -58,10 +55,7 @@ def get_css_urls(bundle, debug=None):
         If True, return URLs for individual files instead of the minified
         bundle.
     """
-    if debug is None:
-        debug = settings.DEBUG
-
-    if debug:
+    if debug or settings.DEBUG or settings.DEV_MODE:
         items = []
         for item in settings.MINIFY_BUNDLES['css'][bundle]:
             should_compile = item.endswith('.less') and getattr(
diff --git a/src/olympia/lib/settings_base.py b/src/olympia/lib/settings_base.py
index 77aef212aa9f..b38d3e6f44b6 100644
--- a/src/olympia/lib/settings_base.py
+++ b/src/olympia/lib/settings_base.py
@@ -59,6 +59,19 @@ def path(*folders):
 
 DEBUG = env('DEBUG', default=False)
 
+# Do NOT provide a default value, this should be explicitly
+# set during the docker image build. If it is not set,
+# we want to raise an error.
+DOCKER_TARGET = env('DOCKER_TARGET')
+
+DEV_MODE = False
+
+# Used to determine if django should serve static files.
+# For local deployments we want nginx to proxy static file requests to the
+# uwsgi server and not try to serve them locally.
+# In production, nginx serves these files from a CDN.
+SERVE_STATIC_FILES = False
+
 DEBUG_TOOLBAR_CONFIG = {
     # Deactivate django debug toolbar by default.
     'SHOW_TOOLBAR_CALLBACK': lambda request: DEBUG,
@@ -699,7 +712,7 @@ def get_db_config(environ_var, atomic_requests=True):
             'js/stats/table.js',
             'js/stats/stats.js',
         ),
-        # This is included when DEBUG is True.  Bundle in <head>.
+        # This is included when DEV_MODE is True.  Bundle in <head>.
         'debug': (
             'js/debug/less_setup.js',
             'less/dist/less.js',
@@ -1316,7 +1329,7 @@ def read_only_mode(env):
     STATIC_BUILD_PATH,
 )
 
-STATICFILES_STORAGE = 'olympia.lib.storage.ManifestStaticFilesStorageNotMaps'
+STATICFILES_STORAGE = 'olympia.lib.storage.OlympiaStaticFilesStorage'
 
 # Path related settings. In dev/stage/prod `NETAPP_STORAGE_ROOT` environment
 # variable will be set and point to our NFS/EFS storage
diff --git a/src/olympia/lib/storage.py b/src/olympia/lib/storage.py
index 0413ca12fc2c..046f1480aeb3 100644
--- a/src/olympia/lib/storage.py
+++ b/src/olympia/lib/storage.py
@@ -1,4 +1,8 @@
-from django.contrib.staticfiles.storage import ManifestStaticFilesStorage
+from django.conf import settings
+from django.contrib.staticfiles.storage import (
+    ManifestStaticFilesStorage,
+    StaticFilesStorage,
+)
 
 
 class ManifestStaticFilesStorageNotMaps(ManifestStaticFilesStorage):
@@ -17,3 +21,8 @@ class ManifestStaticFilesStorageNotMaps(ManifestStaticFilesStorage):
             ),
         ),
     )
+
+
+OlympiaStaticFilesStorage = (
+    StaticFilesStorage if settings.DEV_MODE else ManifestStaticFilesStorageNotMaps
+)
diff --git a/src/olympia/templates/base.html b/src/olympia/templates/base.html
index cdf195eb33cb..cf2b20b8196a 100644
--- a/src/olympia/templates/base.html
+++ b/src/olympia/templates/base.html
@@ -32,7 +32,7 @@
 
     <noscript><link rel="stylesheet" href="{{ static('css/legacy/nojs.css') }}"></noscript>
 
-    {% if settings.DEBUG %}
+    {% if settings.DEV_MODE %}
       {% if settings.LESS_LIVE_REFRESH %}
         <meta id="live_refresh" name="live_refresh" value="1">
       {% endif %}
diff --git a/src/olympia/urls.py b/src/olympia/urls.py
index a00f1da5bfbe..d683cd185218 100644
--- a/src/olympia/urls.py
+++ b/src/olympia/urls.py
@@ -109,11 +109,18 @@
     ),
 ]
 
-if settings.DEBUG:
+if settings.SERVE_STATIC_FILES:
     from django.contrib.staticfiles.views import serve as static_serve
 
     def serve_static_files(request, path, **kwargs):
-        return static_serve(request, path, insecure=True, **kwargs)
+        if settings.DEV_MODE:
+            return static_serve(
+                request, path, insecure=True, show_indexes=True, **kwargs
+            )
+        else:
+            return serve_static(
+                request, path, document_root=settings.STATIC_ROOT, **kwargs
+            )
 
     # Remove leading and trailing slashes so the regex matches.
     media_url = settings.MEDIA_URL.lstrip('/').rstrip('/')