[Python] Django Static Files Not Loading in Production (DEBUG=False) with Gunicorn on...

Problem

I'm running a Django application in a Kubernetes pod with Gunicorn, and my static files (admin panel CSS/JS) are not loading when DEBUG=False.

In local development, I use runserver, and everything works fine with DEBUG=True. However, when I set DEBUG=False, my static files return 404.

Error Logs (Browser Console / Django Logs)

GET /static/admin/css/base.efb520c4bb7c.css HTTP/1.1" 404 179
GET /static/admin/js/nav_sidebar.7605597ddf52.js HTTP/1.1" 404 179


Relevant Django Settings (settings.py)

DEBUG = False

INSTALLED_APPS = [
"django.contrib.staticfiles",
# Other apps...
]

MIDDLEWARE = [
'django.middleware.security.SecurityMiddleware',
'whitenoise.middleware.WhiteNoiseMiddleware',
# Other middleware...
]


BASE_DIR = Path(__file__).resolve().parent.parent
STATIC_URL = '/static/'
STATICFILES_STORAGE = "whitenoise.storage.CompressedManifestStaticFilesStorage"
STATICFILES_DIRS = [
BASE_DIR / 'static',
]
STATIC_ROOT = BASE_DIR / 'staticfiles'



How I Run My App (Docker Entrypoint)

#!/bin/sh

APP_PORT=${PORT:-8000}

echo "Migrating database..."
/opt/venv/bin/python manage.py migrate --noinput

echo "Collecting static files..."
/opt/venv/bin/python manage.py collectstatic --noinput
echo "Static files collected"

echo "Starting server..."
/opt/venv/bin/gunicorn secureuri.wsgi:application --bind "0.0.0.0:${APP_PORT}" --workers 1 --access-logfile - --error-logfile - --log-level debug



What I Tried

• 
  Checked that collectstatic is running.
  
  
• 
  Running ls -la staticfiles/admin/css/ shows that files exist inside the container. Tried running Django’s built-in dev server with DEBUG=False
  
  
• 
  Running python manage.py runserver --insecure does not work
  
  
• 
  Checked Gunicorn Logs
  
  
• 
  Gunicorn is running fine, and there are no errors related to static files.
  
  
• 
  Tried adding whitenoise ❌ (Didn’t work)
  

INSTALLED_APPS = [
"whitenoise.runserver_nostatic",
"django.contrib.staticfiles",
]

MIDDLEWARE = [
"whitenoise.middleware.WhiteNoiseMiddleware",
]

• Restarted the pod, but static files still return 404.

Question

1. How can I serve static files correctly when DEBUG=False without using an external service like Nginx or S3?
2. Is there something I’m missing in my Gunicorn/Kubernetes setup?

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