I'd recommend tracing it back to see where the :authenticate_user! is causing the application to fail.

If i'm stuck on an issue like this, I will sometimes put a debugger log in each controller action with the name of the action. Viewing the logs, you'd be able to see at which point (or the last point) it was able to make its way through before it returned the error. I'm definitely not suggesting to expose the app! That would be bad, but certain controllers need to have unauthenticated access so that it is able to perform the authentication. I'm a big fan of puts debugging. It's similar to rubber duck debugging.

Side note: if you're working on some kind of calculation that is rather difficult and you don't have the tests built yet or is a part of the app where tests will not be created, using a tail | grep can be very handy as well. So in the app, you might have something like

Rails.logger.info "DEBUG:: #{some var}" 

and in your console, do

tail -f log/development.log | grep DEBUG