im not really sure where to start with this one - the menus only popup after a hover event which clearly cant happen simultaneously on all menus. You could try looking at the code via F12 (IE /chrome) or firebug (firefox) to see if you can see the events being fired to track down what it might be. As an alternative you could replace the actions menu control with http://dnnmoduleactions.codeplex.com/ to see if that has the same problem. Finally, it might be an idea to check the site with a validator http://validator.w3.org/ just in case some broken html/script is causing this (very bizarre) issue

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I would prefer to keep a vanilla install as much as possible. Could there possibly be some difference between the install and upgrade packages that is causing this behavior? I haven't experienced it at all with the fresh installs of DNN6, just the upgrades. I even copied my working skins from a fresh install over to an upgraded install and they act the same way. Very bizarre.

I'm not sure what to look for inside of Firebug, but I didn't see anything crazy jump out at me. I did end up finding a workaround though. I simply added the following lines of code at the bottoms of my skins and the pages now load with the module menus collapsed as expected. They also open as expected when hovered upon.