…the OS 9 partition will show in the OF boot loader at Opt+Boot, but it won't actually load (shows the happy mac and then a question mark folder) until I rebless the system folder.
My first guess is that there's something "wrong" with the folder hierarchy. The System file and the Finder file must reside side-by-side in the System Folder at the root / top level of the OS9 partition (which you very probably know) and you "rebless" a System by simply yanking it out of the folder and putting it back.
The happy Mac means the computer knows there's a OS9 System available. The ? means it can't find it when it goes to fetch it.
The clue is that it happens every time you use OSX. Here's where we enter the Twilight Zone where, as above, people tell you that having OSX and OS9 on the same computer, in the same room, in the same country etc etc will cause the world to end. While their paranoia is understandable, given the mysterious nature of the problems that can develop (just like what is happening to you) you can cure it very easily.
What's most likely happening is that OSX is writing stuff on the OS9 partition that is screwing up the OS9 directory. The two bad OSX actors that cause this are Spotlight and Time Machine. Since you have 10.4, you're problem is Spotlight. What happens is Spotlight indexes the OS9 drive and writes it
in the OS9 partition,
in the OS9 directory area. OS9 looks at this and sees it as gobbledegook instead of a readable directory. This wasn't "supposed" to happen… remember, Apple wanted you to move on from the Mac OS into OSX and use Classic if you had OS9 apps you couldn't / wouldn't give up.
The solution is: Boot into OSX, immediately go to System Preferences / Spotlight / Privacy and prevent Spotlight from searching the entire OS9 partition. Restart and go back to OS9. If it won't start, re-bless your System one last time (this depends on how long it took you to shut Spotlight off since it starts re-indexing the OS9 drive immediately when you boot OSX). That's it, end of issue. There is a chance you may ultimately have to re-install OS9 because what you have now is
still a directory that's still messed up with Spotlight data in it. A pass with Disk Warrior at least, won't hurt and is advisable, although it may work fine forever without.
Actually, this usually causes even bigger problems than you're having where the OS's start fighting with each other trying to "fix" the OS9 directory with their respective disk utilities. So, there is a small chance that something
else is wrong but I doubt it and I think this is all you need to do.
Note re above:
I don't guess you're using Classic at all, but if by some chance you are, it should have its own OS9 System on the 10.4 partition and that's another thing entirely.