This is not an answer. This is debugging info, because the comment thread is getting long.
Update: I observed the following on Firefox 3.6 and IE 8 (I know, corporate IT isn't up on the latest versions) on Windows XP. I am not seeing this problem at home with Firefox 13 or Safari 5.1.7 on OS 10.6. (end update)
This shifting happens to me on both beta and graduated sites, but not universally. It does not happen with this user on Workspace, but it does happen wtih another user on the same site. It does not happen when Ben Brocka views that same user.
It happens to me with my own profile on: EL&U, Mi Yodeya, The Workspace, Music, Biblical Hermeneutics, Writers, Board and Card Games. It was happening on UX at the time I posted this but was not doing it several hours later. (It was still doing it on other sites, though.)
I use browser settings (Firefox ctrl-+) to increase the font sizes on these sites. In a test on Mi Yodeya, if I reduce the font three notches (3x ctrl--) the problem goes away, but I can't read text that small. I turned of Stylish to make sure no style overrides were causing this; no difference. I'm not using anything else that should affect rendering on SE.
My browser window is not quite as wide as the site design wants it to be, but it's not tiny. I was once told that the site assumes 1024px width; if so, then eyeballing, I'm probably at about 900px.
Everything I've written is about Firefox. I just tried Rarity's Workspace profile in IE and it worked there. The SE site design apparently does not respond to the IE font directive (Text -> Larger/Largest) and ctrl-+ zooms the entire page, not just the fonts, so I apparently can't create an equivalent situation using that browser. (Whole-page zoom means horizontal scrolling, which is one reason I avoid IE.)
Ben's browser, browser size, and font zoom level are as yet unknown.
Finally, when I visit a page with the broken formatting, I very briefly see it with the correct formatting and then it redraws. I'm not sure what that means.