I already posted this question on Stackoverflow (http://stackoverflow.com/q/33189728/855050), but haven't received any answers, just a comment by another user with the same issue. I am posting here for added visibility. I think this is a bug in Django v1.8. I'll copy the question's text here for convenience.
I wasn't able to produce a minimal example of what was going on, but it is fixed now. Essentially, I did the following:
python manage.py collectstatic
(as suggested in https://community.webfaction.com/questions/18544/there-is-not-popup-window-for-one-to-many-relationship-with-djangos-admin-v18)I hope this is useful to someone else.