Why would django fail with server 500 only when Debug=False AND db is set to production database on Heroku?

Question

When we run $ python manage.py runserver --settings=project.settings.local there are 4 different possible combinations:

1. Debug=True && DB=l

Answer 1

The solution for me was to run python manage.py collectstatic.

If you run $ heroku logs --tail inside terminal before doing this, the log will tell you what static files cannot be found (404).