Oh Gods, where to start? I am also seeing too many games that can't be called Cult Classics, one because they aren't exactly Cult, and some because they aren't that old, so can't be classic.. But I'll try and avoid that..
One I'm a little surprised not to see Monster Hunter, although really popular in Japan (but apparently waning a little over there) they're still releasing the new versions over here because of the cult following it has gained after the first. Think it's presence got a bit squashed by Shadow of the Collossus.
X-Com, Enemy Unknown, Terror from the Deep, and Apocalypse. A dominating force in the Squad Command genre, from what I know pretty much set the style for the genre. I still play today and all.
X-Com's spiritual successor; UFO and it's 2 sequels, still has a few people making mods for it.
The X universe of games
Definitely the Homeworld series, people are still, even now, making mods for number 2.
Vagrant Story. Still to this day has had one of the best antagonists I've seen.
StarTopia. An amazing game, so fun to play. Barely sold and caused Muckyfoot to close more or less. I blame Edios, they didn't give them any money for marketing and thus it hit the shelves without even a whisper. Luck it caught my eye (and ran on my old knackered rig at the time..) People should check it out if you like Dungeon Keeper and it's ilk.
I'm sure I'll think of more later..