diff --git a/Dockerfile b/Dockerfile
index 21dcad79a82..9dfdaf7feb1 100644
--- a/Dockerfile
+++ b/Dockerfile
@@ -10,13 +10,24 @@ ENV BUILD_INFO=/build-info.json
 SHELL ["/bin/bash", "-xue", "-c"]
 
 ENV OLYMPIA_UID=9500
+# give olympia access to the HOME directory
+ENV HOME=/data/olympia
+ENV DEPS_DIR=${HOME}/deps
+ENV NPM_DEPS_DIR=${HOME}/node_modules
+
 RUN <<EOF
 groupadd -g ${OLYMPIA_UID} olympia
-useradd -u ${OLYMPIA_UID} -g ${OLYMPIA_UID} -s /sbin/nologin -d /data/olympia olympia
+useradd -u ${OLYMPIA_UID} -g ${OLYMPIA_UID} -s /sbin/nologin -d ${HOME} olympia
+
+# Create and chown olympia directories
+olympia_dirs=("${DEPS_DIR}" "${NPM_DEPS_DIR}" "${HOME}/storage")
+for dir in "${olympia_dirs[@]}"; do
+  mkdir -p ${dir}
+  chown -R olympia:olympia ${dir}
+done
 EOF
 
-# give olympia access to the HOME directory
-ENV HOME=/data/olympia
+
 WORKDIR ${HOME}
 RUN chown -R olympia:olympia ${HOME}
 
@@ -74,37 +85,28 @@ ENV LANG=en_US.UTF-8
 ENV LC_ALL=en_US.UTF-8
 
 RUN <<EOF
-# Create directory for dependencies
-mkdir /deps
-chown -R olympia:olympia /deps
-
-
 # For backwards-compatibility purposes, set up links to uwsgi. Note that
 # the target does not exist yet at this point, but it will later.
-ln -s /deps/bin/uwsgi /usr/bin/uwsgi
+ln -s ${DEPS_DIR}/bin/uwsgi /usr/bin/uwsgi
 ln -s /usr/bin/uwsgi /usr/sbin/uwsgi
 
-# Create the storage directory and the test file to verify nginx routing
-mkdir -p ${HOME}/storage
-chown -R olympia:olympia ${HOME}/storage
 EOF
 
 USER olympia:olympia
 
 ENV PIP_USER=true
-ENV PIP_BUILD=/deps/build/
-ENV PIP_CACHE_DIR=/deps/cache/
-ENV PIP_SRC=/deps/src/
-ENV PYTHONUSERBASE=/deps
+ENV PIP_BUILD=${DEPS_DIR}/build/
+ENV PIP_CACHE_DIR=${DEPS_DIR}/cache/
+ENV PIP_SRC=${DEPS_DIR}/src/
+ENV PYTHONUSERBASE=${DEPS_DIR}
 ENV PATH=$PYTHONUSERBASE/bin:$PATH
-ENV NPM_CONFIG_PREFIX=/deps/
-ENV NPM_CACHE_DIR=/deps/cache/npm
+ENV NPM_CACHE_DIR=${DEPS_DIR}/cache/npm
 ENV NPM_DEBUG=true
 # Set python path to the project root and src to resolve olympia modules correctly
 ENV PYTHONPATH=${HOME}:${HOME}/src
 
 ENV PIP_COMMAND="python3 -m pip"
-ENV NPM_ARGS="--prefix ${NPM_CONFIG_PREFIX} --cache ${NPM_CACHE_DIR} --loglevel verbose"
+ENV NPM_ARGS="--cache ${NPM_CACHE_DIR} --loglevel verbose"
 
 # All we need in "base" is pip to be installed
 #this let's other layers install packages using the correct version.
@@ -127,7 +129,7 @@ COPY docker/etc/mime.types /etc/mime.types
 
 # 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.
+# and makes copying the /data/olympia/deps dir to the final layer easy.
 FROM base AS pip_production
 
 RUN \
@@ -135,8 +137,8 @@ RUN \
     # Files required to install pip dependencies
     --mount=type=bind,source=./requirements/prod.txt,target=${HOME}/requirements/prod.txt \
     # Files required to install npm dependencies
-    --mount=type=bind,source=package.json,target=/deps/package.json \
-    --mount=type=bind,source=package-lock.json,target=/deps/package-lock.json \
+    --mount=type=bind,source=package.json,target=${HOME}/package.json \
+    --mount=type=bind,source=package-lock.json,target=${HOME}/package-lock.json \
     # Mounts for caching dependencies
     --mount=type=cache,target=${PIP_CACHE_DIR},uid=${OLYMPIA_UID},gid=${OLYMPIA_UID} \
     --mount=type=cache,target=${NPM_CACHE_DIR},uid=${OLYMPIA_UID},gid=${OLYMPIA_UID} \
@@ -146,6 +148,9 @@ EOF
 
 FROM base AS development
 
+# Copy build info from info
+COPY --from=info ${BUILD_INFO} ${BUILD_INFO}
+
 FROM base AS locales
 ARG LOCALE_DIR=${HOME}/locale
 # Compile locales
@@ -155,7 +160,7 @@ COPY --chown=olympia:olympia locale ${LOCALE_DIR}
 RUN \
     --mount=type=bind,source=requirements/locale.txt,target=${HOME}/requirements/locale.txt \
     --mount=type=bind,source=Makefile-docker,target=${HOME}/Makefile-docker \
-    --mount=type=bind,source=locale/compile-mo.sh,target=${HOME}/compile-mo.sh \
+    --mount=type=bind,source=scripts/compile_locales.py,target=${HOME}/scripts/compile_locales.py \
     make -f Makefile-docker compile_locales
 
 # More efficient caching by mounting the exact files we need
@@ -175,10 +180,10 @@ COPY --chown=olympia:olympia static/ ${HOME}/static/
 RUN \
     --mount=type=bind,src=src,target=${HOME}/src \
     --mount=type=bind,src=Makefile-docker,target=${HOME}/Makefile-docker \
+    --mount=type=bind,src=scripts/update_assets.py,target=${HOME}/scripts/update_assets.py \
     --mount=type=bind,src=manage.py,target=${HOME}/manage.py \
 <<EOF
-echo "from olympia.lib.settings_base import *" > settings_local.py
-DJANGO_SETTINGS_MODULE="settings_local" make -f Makefile-docker update_assets
+make -f Makefile-docker update_assets
 EOF
 
 FROM base AS production
@@ -194,4 +199,4 @@ COPY --from=info ${BUILD_INFO} ${BUILD_INFO}
 # Copy compiled locales from builder
 COPY --from=locales --chown=olympia:olympia ${HOME}/locale ${HOME}/locale
 # Copy dependencies from `pip_production`
-COPY --from=pip_production --chown=olympia:olympia /deps /deps
+COPY --from=pip_production --chown=olympia:olympia ${DEPS_DIR} ${DEPS_DIR}
diff --git a/Makefile-docker b/Makefile-docker
index 87c2ef8c6bc..a329887349b 100644
--- a/Makefile-docker
+++ b/Makefile-docker
@@ -8,16 +8,6 @@ export PYTHON_COMMAND=python3
 export PIP_COMMAND=$(PYTHON_COMMAND) -m pip
 APP=src/olympia/
 
-NODE_MODULES := $(NPM_CONFIG_PREFIX)node_modules/
-
-REQUIRED_FILES := \
-	Makefile \
-	Makefile-os \
-	Makefile-docker \
-	/deps/package.json \
-	/deps/package-lock.json \
-	/addons-server-docker-container \
-
 # Build list of dependencies to install
 DEPS = pip prod
 # If we're running a development image, then we should install the development dependencies
@@ -72,14 +62,8 @@ data_load:
 	./manage.py data_load $(ARGS)
 
 .PHONY: update_assets
-update_assets:
-	# Copy files required in compress_assets to the static folder
-	# If changing this here, make sure to adapt tests in amo/test_commands.py
-	$(PYTHON_COMMAND) manage.py compress_assets
-	$(PYTHON_COMMAND) manage.py generate_jsi18n_files
-	# Collect static files: This MUST be run last or files will be missing
-	$(PYTHON_COMMAND) manage.py collectstatic --noinput
-
+update_assets: ## Update the static assets
+	$(HOME)/scripts/update_assets.py
 
 .PHONY: update_deps
 update_deps: ## Update the dependencies
@@ -94,7 +78,7 @@ setup-ui-tests:
 lint: ## lint the code
 	ruff check .
 	ruff format --check .
-	NODE_PATH=$(NODE_MODULES) npm exec $(NPM_ARGS) -- prettier --check '**'
+	npm exec $(NPM_ARGS) -- prettier --check '**'
 	curlylint src/
 
 lint-codestyle: lint
@@ -199,15 +183,15 @@ test_failed: ## rerun the failed tests from the previous run
 
 .PHONY: run_js_tests
 run_js_tests: ## Run the JavaScript test suite (requires compiled/compressed assets).
-	NODE_PATH=$(NODE_MODULES) npm exec $(NPM_ARGS) -- jest tests/js
+	npm exec $(NPM_ARGS) -- jest tests/js
 
 .PHONY: watch_js_tests
 watch_js_tests: ## Run+watch the JavaScript test suite (requires compiled/compressed assets).
-	NODE_PATH=$(NODE_MODULES) npm exec $(NPM_ARGS) -- jest --watch
+	npm exec $(NPM_ARGS) -- jest --watch
 
 .PHONY: format
 format: ## Autoformat our codebase.
-	NODE_PATH=$(NODE_MODULES) npm exec $(NPM_ARGS) -- prettier --write '**'
+	npm exec $(NPM_ARGS) -- prettier --write '**'
 	ruff check --fix-only .
 	ruff format .
 
@@ -218,7 +202,7 @@ extract_locales: ## extracts and merges translation strings
 .PHONE: compile_locales
 compile_locales: ## compiles translation strings
 	$(PIP_COMMAND) install --progress-bar=off --no-deps -r requirements/locale.txt
-	./locale/compile-mo.sh ./locale/
+	$(HOME)/scripts/compile_locales.py
 
 .PHONY: help_submake
 help_submake:
diff --git a/Makefile-os b/Makefile-os
index e3079503fcd..1eba7b16701 100644
--- a/Makefile-os
+++ b/Makefile-os
@@ -153,17 +153,17 @@ docker_clean_build_cache: ## Remove buildx build cache
 .PHONY: clean_docker
 clean_docker: docker_compose_down docker_mysqld_volume_remove docker_clean_images docker_clean_volumes docker_clean_build_cache ## Remove all docker resources taking space on the host machine
 
-.PHONY: docker_update_deps
-docker_update_deps: docker_mysqld_volume_create ## Update the dependencies in the container based on the docker tag and target
+.PHONY: docker_sync_host
+docker_sync_host: docker_mysqld_volume_create ## Update the dependencies in the container based on the docker tag and target
 	docker compose run \
 		--rm \
 		--no-deps \
 		$(DOCKER_RUN_ARGS) \
 		web \
-		make update_deps
+		./scripts/sync_host_files.py
 
 .PHONY: up_pre
-up_pre: setup docker_pull_or_build docker_update_deps ## Pre-up the environment, setup files, volumes and host state
+up_pre: setup docker_pull_or_build docker_sync_host ## Pre-up the environment, setup files, volumes and host state
 
 .PHONY: up_start
 up_start: docker_mysqld_volume_create ## Start the docker containers
diff --git a/docker-compose.yml b/docker-compose.yml
index 4e847cacc98..27a7d852013 100644
--- a/docker-compose.yml
+++ b/docker-compose.yml
@@ -46,9 +46,9 @@ services:
     volumes:
       # used by: web, worker, nginx
       - ${HOST_MOUNT_SOURCE:?}:/data/olympia
-      - ${HOST_MOUNT_SOURCE:?}deps:/deps
-      - data_site_static:/data/olympia/site-static
-      - ${HOST_MOUNT_SOURCE:?}storage:/data/olympia/storage
+      - ${HOST_MOUNT_SOURCE:?}deps:/data/olympia/deps
+      - ./site-static:/data/olympia/site-static
+      - ./storage:/data/olympia/storage
   worker:
     <<: *olympia
     command: [
@@ -64,8 +64,8 @@ services:
     ]
     volumes:
       - ${HOST_MOUNT_SOURCE:?}:/data/olympia
-      - ${HOST_MOUNT_SOURCE:?}deps:/deps
-      - ${HOST_MOUNT_SOURCE:?}storage:/data/olympia/storage
+      - ${HOST_MOUNT_SOURCE:?}deps:/data/olympia/deps
+      - ./storage:/data/olympia/storage
     extra_hosts:
      - "olympia.test:127.0.0.1"
     restart: on-failure:5
diff --git a/docker/entrypoint.sh b/docker/entrypoint.sh
index e3f59fcdc48..1a8bf6764fd 100755
--- a/docker/entrypoint.sh
+++ b/docker/entrypoint.sh
@@ -30,10 +30,10 @@ fi
 NEW_HOST_UID=$(get_olympia_uid)
 OLYMPIA_ID_STRING="${NEW_HOST_UID}:$(get_olympia_gid)"
 
-# If we are on production mode, update the ownership of /data/olympia and /deps to match the new id
+# If we are on production mode, update the ownership of /data/olympia to match the new id
 if [[ "${HOST_MOUNT}" == "production" ]]; then
-  echo "Updating ownership of /data/olympia and /deps to ${OLYMPIA_ID_STRING}"
-  chown -R ${OLYMPIA_ID_STRING} /data/olympia /deps
+  echo "Updating ownership of /data/olympia to ${OLYMPIA_ID_STRING}"
+  chown -R ${OLYMPIA_ID_STRING} /data/olympia
 fi
 
 cat <<EOF | su -s /bin/bash $OLYMPIA_USER
diff --git a/docs/topics/development/building_and_running_services.md b/docs/topics/development/building_and_running_services.md
index 364b81225dd..9e9efdbe10c 100644
--- a/docs/topics/development/building_and_running_services.md
+++ b/docs/topics/development/building_and_running_services.md
@@ -14,7 +14,7 @@ The Dockerfile for the **addons-server** project uses a multi-stage build to opt
 
 3. **Mounts in Docker Compose**:
    - **Mounting Local Repository**: The volume `.:/data/olympia` mounts the local Git repository into the container, allowing real-time changes to files within the container.
-   - **Mounting Dependencies**: The volume `./deps:/deps` mounts the dependencies directory, enabling better caching across builds and providing visibility for debugging directly on the host.
+   - **Mounting Dependencies**: The volume `./deps:/data/olympia/deps` mounts the dependencies directory, enabling better caching across builds and providing visibility for debugging directly on the host.
 
 4. **Environment Variables for OLYMPIA_USER**:
    - **Development Setup**: The `OLYMPIA_UID` .env variable is set to the host user ID, ensuring that the container runs with the correct permissions.
@@ -178,4 +178,4 @@ Additionally this volume is "external" to allow the volume to persist across con
 We additionally mount serval local directories to the web/worker containers.
 
 - **.:/data/olympia**: Mounts the local repository into the container to allow real-time changes to files within the container.
-- **./deps:/deps**: Mounts the dependencies directory to enable better caching across builds and provide visibility for debugging directly on the host.
+- **./deps:/data/olympia/deps**: Mounts the dependencies directory to enable better caching across builds and provide visibility for debugging directly on the host.
diff --git a/docs/topics/development/dependency_management.md b/docs/topics/development/dependency_management.md
index 7f73bd19bc6..483e99c468d 100644
--- a/docs/topics/development/dependency_management.md
+++ b/docs/topics/development/dependency_management.md
@@ -4,9 +4,9 @@ Managing dependencies effectively is crucial for maintaining a stable and consis
 
 ## Python Dependencies
 
-Python dependencies are managed using the Makefile and requirements files. All dependencies are installed into the `/deps` directory, which centralizes dependency management and simplifies data mounts.
+Python dependencies are managed using the Makefile and requirements files. All dependencies are installed into the `/data/olympia/deps` directory, which centralizes dependency management and simplifies data mounts.
 
-- **Environment Variables**: The project sets environment variables for Python CLIs to install dependencies in specific locations. This includes setting paths for `PIP_CACHE_DIR`, `PIP_SRC`, and others to use the `/deps` directory.
+- **Environment Variables**: The project sets environment variables for Python CLIs to install dependencies in specific locations. This includes setting paths for `PIP_CACHE_DIR`, `PIP_SRC`, and others to use the `/data/olympia/deps` directory.
 
 - **Caching Mechanism**: By using Docker build stages, the project isolates the stages responsible for installing dependencies. This prevents these stages from re-running unless the actual dependency files are changed. Additionally, internal Python cache folders are cached, avoiding unnecessary re-downloads of packages and saving time and bandwidth.
 
@@ -66,9 +66,7 @@ Ensure to comment in the requirements file above transitive dependencies which d
 
 ## Node.js Dependencies
 
-Node.js dependencies are managed using npm. Similar to Python dependencies, Node.js dependencies are installed into the `/deps` directory.
-
-- **Environment Variables**: Environment variables are set for Node.js CLIs to ensure that dependencies are installed in the `/deps` directory. This includes setting paths for `NPM_CONFIG_PREFIX` and `NPM_CACHE_DIR`.
+Node.js dependencies are managed using npm.
 
 - **Caching Mechanism**: Node.js dependencies are also cached using Docker build stages. Internal npm cache folders are cached to avoid re-downloading packages unnecessarily.
 
@@ -86,19 +84,19 @@ NPM is a fully-featured package manager, so you can use the standard CLI.
 
 The Dockerfile uses build stages to isolate the dependency installation process. This ensures that stages do not re-run unless the dependency files themselves change. The caching mechanism includes:
 
-- **Dependency Cache**: Both Python and Node.js dependencies are cached in the `/deps` directory.
+- **Dependency Cache**: Both Python and Node.js dependencies are cached in the `/data/olympia/deps` directory.
 - **Cache Folders**: Internal cache folders for pip and npm are themselves cached to speed up the build process.
 
 ## GitHub Actions Cache
 
-The project uses a custom GitHub Actions action (`./.github/actions/cache-deps`) to cache the `/deps` folder. This action significantly increases install times for CI runs by leveraging the GitHub Actions cache.
+The project uses a custom GitHub Actions action (`./.github/actions/cache-deps`) to cache the `/data/olympia/deps` folder. This action significantly increases install times for CI runs by leveraging the GitHub Actions cache.
 
 ```yaml
 - name: Cache dependencies
   uses: ./.github/actions/cache-deps
 ```
 
-By caching the `/deps` folder, the project ensures that dependencies are quickly restored in CI environments, reducing overall build and test times.
+By caching the `/data/olympia/deps` folder, the project ensures that dependencies are quickly restored in CI environments, reducing overall build and test times.
 
 ## Updating/Installing Dependencies
 
@@ -109,4 +107,4 @@ make up
 ```
 
 This will rebuild the Docker image with the current dependencies specified in the `requirements` and `package.json` files.
-We do not support updating dependencies in a running container as the /deps folder is not writable by the olympia user.
+We do not support updating dependencies in a running container as the /data/olympia/deps folder is not writable by the olympia user.
diff --git a/docs/topics/development/performance_and_optimization.md b/docs/topics/development/performance_and_optimization.md
index 8cfc2429b0c..6f812536973 100644
--- a/docs/topics/development/performance_and_optimization.md
+++ b/docs/topics/development/performance_and_optimization.md
@@ -28,7 +28,7 @@ Docker layer caching is a powerful feature that significantly speeds up the buil
      export DOCKER_BUILDKIT=1
      ```
 
-   - **GitHub Actions Cache**: The custom action (`./.github/actions/cache-deps`) caches the `/deps` folder, leveraging GitHub Actions cache to improve CI run times.
+   - **GitHub Actions Cache**: The custom action (`./.github/actions/cache-deps`) caches the `/data/olympia/deps` folder, leveraging GitHub Actions cache to improve CI run times.
 
 ## Performance Testing
 
diff --git a/locale/compile-mo.sh b/locale/compile-mo.sh
deleted file mode 100755
index d50a894a7f1..00000000000
--- a/locale/compile-mo.sh
+++ /dev/null
@@ -1,37 +0,0 @@
-#!/bin/bash
-# syntax:
-# compile-mo.sh locale-dir/
-
-# Make this script fail if any command exits wit exit code != 0
-set -ue
-
-function process_po_file() {
-    pofile=$1
-    dir=$(dirname "$pofile")
-    lang=$(echo "$pofile" | cut -d "/" -f2)
-    stem=$(basename "$pofile" .po)
-    touch "${dir}/${stem}.mo"
-    dennis-cmd lint --errorsonly "$pofile" && msgfmt -o "${dir}/${stem}.mo" "$pofile"
-}
-
-# We are spawning sub processes with `xargs`
-# and the function needs to be available in that sub process
-export -f process_po_file
-
-function usage() {
-    echo "syntax:"
-    echo "compile-mo.sh locale-dir/"
-    exit 1
-}
-
-# check if file and dir are there
-if [[ ($# -ne 1) || (! -d "$1") ]]; then usage; fi
-
-# Ensure dennis-cmd cli is available in the environment
-hash dennis-cmd
-
-echo "compiling django.po..."
-find $1 -type f -name "django.po" -print0 | xargs -0 -n1 -P4 bash -c 'process_po_file "$@"' _
-
-echo "compiling djangojs.po..."
-find $1 -type f -name "djangojs.po" -print0 | xargs -0 -n1 -P4 bash -c 'process_po_file "$@"' _
diff --git a/pyproject.toml b/pyproject.toml
index f5487e3c483..ccbf08cea9e 100644
--- a/pyproject.toml
+++ b/pyproject.toml
@@ -27,6 +27,8 @@ classifiers = [
 
 [tool.ruff]
 exclude = [
+    "deps",
+    "node_modules",
     "docs",
     "static",
     ".git",
diff --git a/scripts/compile_locales.py b/scripts/compile_locales.py
new file mode 100755
index 00000000000..17e0e663cbc
--- /dev/null
+++ b/scripts/compile_locales.py
@@ -0,0 +1,71 @@
+#!/usr/bin/env python3
+
+import os
+import subprocess
+from concurrent.futures import ThreadPoolExecutor
+
+
+def process_po_file(pofile, attempt=0):
+    """Process a single .po file, creating corresponding .mo file."""
+    print('processing', pofile)
+    directory = os.path.dirname(pofile)
+    stem = os.path.splitext(os.path.basename(pofile))[0]
+    mo_path = os.path.join(directory, f'{stem}.mo')
+
+    # Touch the .mo file
+    open(mo_path, 'a').close()
+
+    try:
+        # Run dennis-cmd lint
+        subprocess.run(
+            ['dennis-cmd', 'lint', '--errorsonly', pofile],
+            capture_output=True,
+            check=False,
+        )
+        # If lint passes, run msgfmt
+        subprocess.run(['msgfmt', '-o', mo_path, pofile], check=True)
+        return
+    except subprocess.CalledProcessError as e:
+        if attempt < 3:
+            print(f'Failed attempt {attempt} for {pofile}, retrying...')
+            return process_po_file(pofile, attempt=attempt + 1)
+        raise e
+
+
+def main():
+    # Ensure 'dennis' is installed
+    try:
+        import dennis as _
+    except ImportError:
+        print(
+            'Error: dennis is not installed. Please install it with pip install dennis'
+        )
+        exit(1)
+
+    locale_dir = os.path.abspath(
+        os.path.join(
+            os.path.dirname(__file__),
+            '..',
+            'locale',
+        )
+    )
+
+    print(f'Compiling locales in {locale_dir}')
+
+    # Collect all files first
+    django_files = []
+    djangojs_files = []
+    for root, _, files in os.walk(locale_dir):
+        for file in files:
+            if file == 'django.po':
+                django_files.append(os.path.join(root, file))
+            elif file == 'djangojs.po':
+                djangojs_files.append(os.path.join(root, file))
+
+    # Process django.po files in parallel
+    with ThreadPoolExecutor() as executor:
+        executor.map(process_po_file, django_files + djangojs_files)
+
+
+if __name__ == '__main__':
+    main()
diff --git a/scripts/install_deps.py b/scripts/install_deps.py
index 5ef16dbbfb8..f8c0352a0a4 100755
--- a/scripts/install_deps.py
+++ b/scripts/install_deps.py
@@ -6,13 +6,14 @@
 import sys
 
 
-def copy_package_json():
-    """Copy package.json files to deps directory if they exist."""
-    try:
-        shutil.copy('/data/olympia/package.json', '/deps')
-        shutil.copy('/data/olympia/package-lock.json', '/deps')
-    except (IOError, OSError):
-        pass  # Ignore if files don't exist or can't be copied
+def clean_dir(dir_path, filter):
+    if not os.path.exists(dir_path):
+        return
+
+    for item in os.listdir(dir_path):
+        item_path = os.path.join(dir_path, item)
+        if os.path.isdir(item_path) and item not in filter:
+            shutil.rmtree(item_path)
 
 
 def main(targets):
@@ -21,6 +22,8 @@ def main(targets):
     DOCKER_TAG = os.environ.get('DOCKER_TAG', 'local')
     DOCKER_TARGET = os.environ.get('DOCKER_TARGET', '')
     OLYMPIA_DEPS = os.environ.get('OLYMPIA_DEPS', '')
+    DEPS_DIR = os.environ.get('DEPS_DIR')
+    NPM_DEPS_DIR = os.environ.get('NPM_DEPS_DIR')
 
     if not targets:
         raise ValueError('No targets specified')
@@ -31,23 +34,21 @@ def main(targets):
         f'DOCKER_TAG: {DOCKER_TAG} \n',
         f'DOCKER_TARGET: {DOCKER_TARGET} \n',
         f'OLYMPIA_DEPS: {OLYMPIA_DEPS} \n',
+        f'DEPS_DIR: {DEPS_DIR} \n',
+        f'NPM_DEPS_DIR: {NPM_DEPS_DIR} \n',
     )
 
     # If we are installing production dependencies or on a non local image
     # we always remove existing deps as we don't know what was previously
-    # installed or in the host ./deps directory before running this script
+    # installed or in the host ./deps or ./node_modules directory
+    # before running this script
     if 'local' not in DOCKER_TAG or OLYMPIA_DEPS == 'production':
         print('Removing existing deps')
-        for item in os.listdir('/deps'):
-            item_path = os.path.join('/deps', item)
-            if os.path.isdir(item_path) and item != 'cache':
-                shutil.rmtree(item_path)
+        clean_dir(DEPS_DIR, ['cache'])
+        clean_dir(NPM_DEPS_DIR, [])
     else:
         print('Updating existing deps')
 
-    # Copy package.json files
-    copy_package_json()
-
     # Prepare the includes lists
     pip_includes = []
     npm_includes = []
diff --git a/scripts/sync_host_files.py b/scripts/sync_host_files.py
new file mode 100755
index 00000000000..6ca2154bcee
--- /dev/null
+++ b/scripts/sync_host_files.py
@@ -0,0 +1,22 @@
+#!/usr/bin/env python3
+
+import json
+import os
+import subprocess
+
+
+def main():
+    BUILD_INFO = os.environ.get('BUILD_INFO')
+
+    subprocess.run(['make', 'update_deps'], check=True)
+
+    with open(BUILD_INFO, 'r') as f:
+        build_info = json.load(f)
+
+    if build_info.get('target') == 'production':
+        subprocess.run(['make', 'compile_locales'], check=True)
+        subprocess.run(['make', 'update_assets'], check=True)
+
+
+if __name__ == '__main__':
+    main()
diff --git a/scripts/update_assets.py b/scripts/update_assets.py
new file mode 100755
index 00000000000..91c02ba9178
--- /dev/null
+++ b/scripts/update_assets.py
@@ -0,0 +1,47 @@
+#!/usr/bin/env python3
+
+import os
+import shutil
+import subprocess
+
+
+def main():
+    HOME = os.environ.get('HOME')
+    STATIC_DIRS = ['static-build', 'site-static']
+
+    for dir in STATIC_DIRS:
+        path = os.path.join(HOME, dir)
+        os.makedirs(path, exist_ok=True)
+        for file in os.listdir(path):
+            file_path = os.path.join(path, file)
+            print(f'Removing {file_path}')
+            if os.path.isdir(file_path):
+                shutil.rmtree(file_path)
+            else:
+                os.remove(file_path)
+
+    script_prefix = ['python3', 'manage.py']
+
+    environment = os.environ.copy()
+    # Always run in production mode without any development settings
+    environment['DJANGO_SETTINGS_MODULE'] = 'olympia.lib.settings_base'
+
+    subprocess.run(
+        script_prefix + ['compress_assets'],
+        check=True,
+        env=environment,
+    )
+    subprocess.run(
+        script_prefix + ['generate_jsi18n_files'],
+        check=True,
+        env=environment,
+    )
+    subprocess.run(
+        script_prefix + ['collectstatic', '--noinput'],
+        check=True,
+        env=environment,
+    )
+
+
+if __name__ == '__main__':
+    main()
diff --git a/src/olympia/amo/fixtures/sentry_event.json b/src/olympia/amo/fixtures/sentry_event.json
index 50a99cc8049..26b9c002ea2 100644
--- a/src/olympia/amo/fixtures/sentry_event.json
+++ b/src/olympia/amo/fixtures/sentry_event.json
@@ -114,7 +114,7 @@
         "stacktrace": {
           "frames": [
             {
-              "abs_path": "/deps/lib/python3.9/site-packages/django/core/handlers/exception.py",
+              "abs_path": "/data/olympia/deps/lib/python3.9/site-packages/django/core/handlers/exception.py",
               "context_line": "                response = get_response(request)",
               "filename": "django/core/handlers/exception.py",
               "function": "inner",
@@ -142,7 +142,7 @@
               }
             },
             {
-              "abs_path": "/deps/lib/python3.9/site-packages/django/core/handlers/base.py",
+              "abs_path": "/data/olympia/deps/lib/python3.9/site-packages/django/core/handlers/base.py",
               "context_line": "                response = wrapped_callback(request, *callback_args, **callback_kwargs)",
               "filename": "django/core/handlers/base.py",
               "function": "_get_response",
@@ -175,7 +175,7 @@
               }
             },
             {
-              "abs_path": "/deps/lib/python3.9/site-packages/django/views/decorators/cache.py",
+              "abs_path": "/data/olympia/deps/lib/python3.9/site-packages/django/views/decorators/cache.py",
               "context_line": "        response = view_func(request, *args, **kwargs)",
               "filename": "django/views/decorators/cache.py",
               "function": "_wrapped_view_func",
diff --git a/src/olympia/lib/settings_base.py b/src/olympia/lib/settings_base.py
index 4bd6faee9c2..26387d6c363 100644
--- a/src/olympia/lib/settings_base.py
+++ b/src/olympia/lib/settings_base.py
@@ -98,15 +98,15 @@ def path(*folders):
 # LESS CSS OPTIONS (Debug only).
 LESS_PREPROCESS = True  # Compile LESS with Node, rather than client-side JS?
 LESS_LIVE_REFRESH = False  # Refresh the CSS on save?
-LESS_BIN = env('LESS_BIN', default='/deps/node_modules/less/bin/lessc')
+LESS_BIN = env('LESS_BIN', default=path('node_modules/less/bin/lessc'))
 
 # Path to cleancss (our CSS minifier).
 CLEANCSS_BIN = env(
-    'CLEANCSS_BIN', default='/deps/node_modules/clean-css-cli/bin/cleancss'
+    'CLEANCSS_BIN', default=path('node_modules/clean-css-cli/bin/cleancss')
 )
 
 # Path to our JS minifier.
-JS_MINIFIER_BIN = env('JS_MINIFIER_BIN', default='/deps/node_modules/terser/bin/terser')
+JS_MINIFIER_BIN = env('JS_MINIFIER_BIN', default=path('node_modules/terser/bin/terser'))
 
 # rsvg-convert is used to save our svg static theme previews to png
 RSVG_CONVERT_BIN = env('RSVG_CONVERT_BIN', default='rsvg-convert')
@@ -116,7 +116,7 @@ def path(*folders):
 
 # Path to our addons-linter binary
 ADDONS_LINTER_BIN = env(
-    'ADDONS_LINTER_BIN', default='/deps/node_modules/addons-linter/bin/addons-linter'
+    'ADDONS_LINTER_BIN', default=path('node_modules/addons-linter/bin/addons-linter')
 )
 # --enable-background-service-worker linter flag value
 ADDONS_LINTER_ENABLE_SERVICE_WORKER = False
@@ -1327,11 +1327,11 @@ def read_only_mode(env):
     'django_node_assets.finders.NodeModulesFinder',
 )
 
-NODE_MODULES_ROOT = os.path.join('/', 'deps', 'node_modules')
-NODE_PACKAGE_JSON = os.path.join('/', 'deps', 'package.json')
+NODE_MODULES_ROOT = path('node_modules')
+NODE_PACKAGE_JSON = path('package.json')
 NODE_PACKAGE_MANAGER_INSTALL_OPTIONS = ['--dry-run']
 
-STATIC_BUILD_PATH = os.path.join('/', 'data', 'olympia', 'static-build')
+STATIC_BUILD_PATH = path('static-build')
 
 STATICFILES_DIRS = (
     path('static'),
diff --git a/tests/make/test_install_deps.py b/tests/make/test_install_deps.py
index 2a4d6344b24..6ed42081713 100644
--- a/tests/make/test_install_deps.py
+++ b/tests/make/test_install_deps.py
@@ -1,30 +1,13 @@
 import unittest
 from unittest import mock
 
-from scripts.install_deps import copy_package_json, main
+from scripts.install_deps import main
 from tests import override_env
 
 
-@mock.patch('scripts.install_deps.shutil.copy')
-class TestCopyPackageJson(unittest.TestCase):
-    def test_copy_package_json(self, mock_shutil):
-        copy_package_json()
-        assert mock_shutil.call_args_list == [
-            mock.call('/data/olympia/package.json', '/deps'),
-            mock.call('/data/olympia/package-lock.json', '/deps'),
-        ]
-
-    def test_copy_package_json_no_files(self, mock_shutil):
-        mock_shutil.side_effect = IOError
-        copy_package_json()
-        assert mock_shutil.call_args_list == [
-            mock.call('/data/olympia/package.json', '/deps'),
-        ]
-
-
 class TestInstallDeps(unittest.TestCase):
     def setUp(self):
-        mocks = ['shutil.rmtree', 'os.listdir', 'subprocess.run', 'copy_package_json']
+        mocks = ['shutil.rmtree', 'os.listdir', 'subprocess.run']
         self.mocks = {}
         for mock_name in mocks:
             patch = mock.patch(
@@ -53,6 +36,8 @@ def _test_remove_existing_deps(self, args, expect_remove=False):
         with override_env(
             **{
                 'PIP_COMMAND': 'pip-test',
+                'DEPS_DIR': '/data/olympia/deps',
+                'NPM_DEPS_DIR': '/data/olympia/deps/npm',
                 'NPM_ARGS': 'npm-test',
                 **args,
             }
@@ -62,8 +47,7 @@ def _test_remove_existing_deps(self, args, expect_remove=False):
         if expect_remove:
             assert self.mocks['os.listdir'].called
             assert self.mocks['shutil.rmtree'].call_args_list == [
-                mock.call('/deps/lib'),
-                mock.call('/deps/node_modules'),
+                mock.call('/data/olympia/deps/lib'),
             ]
         else:
             assert not self.mocks['os.listdir'].called
@@ -109,11 +93,6 @@ def test_remove_deps_for_prod_deps_in_prod(self):
         }
         self._test_remove_existing_deps(args, expect_remove=True)
 
-    def test_copy_package_json_called(self):
-        """Test that copy_package_json is called"""
-        main(['prod'])
-        assert self.mocks['copy_package_json'].called
-
     @override_env(PIP_COMMAND='pip-test', NPM_ARGS='npm-test')
     def test_pip_command_set_on_environment(self):
         main(['prod'])
@@ -165,10 +144,8 @@ def test_correct_args_passed_to_subprocesses(self):
                     '--no-save',
                     '--no-audit',
                     '--no-fund',
-                    '--prefix',
-                    '/deps/',
                     '--cache',
-                    '/deps/cache/npm',
+                    '/data/olympia/deps/cache/npm',
                     '--loglevel',
                     'verbose',
                     '--include',