The answer is: yes — color management must be enabled in both places, and the profile must be loaded in each application.

The system-wide profile does two things:

1. Loads the Video LUT at login. This look-up-table includes color temperature and gamma correction, but that's it. (This is via gcm-apply)
2. Provides a way (using colord, on modern systems) for applications to find the system profile.

Then, individual applications must separately have color management enabled. This may or may not be on by default. It was off in Gimp and Inkscape on my Fedora 15 system, but on in the Geeqie quick image viewer. Firefox has it enabled, but only for images with their own embedded profiles — there's a setting to use it for everything.

Then, applications use liblcms to actually apply the XYZ matrix from the profile. This is the real work — the actual correction tables. Most applications seem to have a way to load the system profile automatically, but if you want you can in every case I've found give it a direct path.

In any case, both parts need to be active.

Thanks to Pascal de Bruijn for clearing this up for me on the Gnome Color Manager mailing list.

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Note: one can use the following images to check if your browser or other application is working properly. They use tricks in the color response to make different text show up depending on whether color management is working or not.

— littlecms browser check images

In Firefox 5, I see that it's working, but "not correctly". That's this issue.