Putting drives to sleep is already unchecked, this is not the problem, but thanks for the suggestion anyway.
I believe I have found the issue, it appears that Apple, in their "wisdom" have determined that all external devices should be unmounted when there is no user is logged in. Perhaps this makes sense for some disks, but for Time Machine disks, this is ridiculous in my opinion. Make a bunch of changes and logout, and poof - no backup of your changes until somebody logs in at a future time hours or days later. Sharing your files to another computer? Better log in to the system occasionally to get those changed files backed up, they will not back themselves up you know. Crazy. This should minimally be configurable for TimeMachine, what is the purpose of hourly backups if they don't actually backup hourly. If you're luck enough to have your Time Machine disk internal, then all will work as expected. Too bad for us iMac users.
Luckily I found a 'fix' here: http://systemsboy.com/2008/04/time-machine-after-logout.html
Essentially the following undocumented preference will turn off this behavior:
sudo defaults write /Library/Preferences/SystemConfiguration/autodiskmount AutomountDisksWithoutUserLogin -bool true