Hey mflintjer,
First off I'm using a Mac and haven't learned the difference between Mac and Windows font management. On the Mac I'm using FontAgent Pro which collects all my fonts into one location (except for some vital system fonts) and allows me to organize them into libraries and sets. Between the two, I can access fonts by foundry or a personalized descriptive classes.
I have a start up set of about 150 of my favorite, most often used fonts, in addition to the system fonts which load when my system boots. I then open FAP, choose and activate whichever fonts I wish to use for a project and they are deactivated the next time the computer is shut off. There are strict diagnostic routines as well so each time a font is activated it is checked for integrity.
The net result of using a throroughly professional font manager is that I never am loading more than 300 fonts at once. There are no corrupt font issues. I can organize and survey any number of fonts rapidly, like a movie, for making aesthetic decisions about which font to use, many Adobe applications have a plugin which will auto-activate fonts used in their documents when they are opened and the fonts aren't currently activated and there are many other lesser features.
Frankly, once your font collection exceeds 1000 fonts you need a font manager. Actually, over 500 and it doesn't hurt to think about it.