It does them all at once. The new system knows about interdependencies, so if you have ForeignKeys between apps it'll make all of them in the right order.
Has it solved that issue where say I have a TinyMCE field, then I ditch TinyMCE and use CKEditor, that I'd still need TinyMCE installed in order to do the old migration, despite it just being a TextField database-wise?
So if I understand correctly, "makemigrations" will convert all apps to use migrations except apps which were created using previous versions of Django?
It will prompt you if an app doesn't yet have migrations and ask if you want it to. That prompt is currently a bit aggressive - asking you every time - but that will be fixed soon.