I have a very similar problem. What I ended up figuring out was that when I use the 'nv' driver. The 'nvidia' driver does not have this problem.
** Changed in: Ubuntu
Sourcepackagename: None => xserver-xorg-driver-nv
Status: Unconfirmed => Needs Info
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Ubuntu 6.10 RC LiveCD works on 2nd monitor but not first
https://launchpad.net/bugs/67878
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