Hi John,
So now it sounds like it isn't even related to 51degrees since you removed it from the equation and the problem still happens.
Are you sure its related to recent mojoPortal updates? ie did you upgrade recently and it started right away after that?
My guess is it is more likely the result of changes in a recent ASP.NET security update.
Are you seeing any errors in the log?
The ASP.NET security update set a limit on the allowed number of form elements and your home page has a lot of them so it seems likely a factor. I encountered an error on this site after the security update when I went to save site settings. It turned out to be caused by having too many form elements because I had a lot of roles and the permission tab has about 10-12 checbox lists populated by all the roles and combined with all the other form elements on the page it all added up to more than 1000 form elements which is what the new security update set as a limit. I solved it temporarily by removing extra roles that I was not using, and I have since solved it in our source code repository by moving the permissions out of site settings into its own pages such that only one permission is updated at a time so even with a lot of roles it doesn't add up to that many form elements.
There is another workaround you can try as mentioned in the post by Scott Gu linked above, you can add this in your user.config file
<add key="aspnet:MaxHttpCollectionKeys" value="1500"/>
You may want to experiment with that and try higher numbers like 2000 and if that solves it back it down as much as you can without restoring the error.
I don't see why it would be browser specific though if it is caused by the ASP.NET security update changes, but your home page does have a lot of form elements so that would be my first guess.
Hope that helps,
Joe