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With my two-video-card setup I'm currently forced to run two non-Xinerama desktops side-by-side, each with their own gnome-panels. (When I move my mouse off the edge of one, input focus changes to the next one.) Additionally, sometimes I remote login to a desktop computer and I have two desktops running: one on the console and one connected to the remote terminal.

In both cases, I have not found a web browser that execute on both desktops at the same time. You may have exactly one instance per user per profile, and that instance runs on exactly one desktop -- not two or more. The only workaround is to run different browser profiles on each desktop (i.e. "firefox -profile $path-of-second-profile") and these separate profiles of course never share any data with each other.

I find this multiple-instance restriction with Opera, Firefox, Chrome, Midori, and Konquerer and at this point I've given up. In contrast, tools like Gnome-panel, Gnome-terminal, Nautilus, Thunar, Gedit, and Okular are happy to run multiple instances on different desktops simultaneously.

Is there a browser out there that supports what I want, and fully supports JavaScript, Java, and Flash?

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This might not really be the answer that you are looking for, but since I can't comment (weird restrictions :| ), here goes:

A solution to your problem could be that you sync your userdata between the two browsers. I know that at least Opera (Link), Firefox and Chrome (both Sync) offer it. You connect your user data to an email adress and it is synced automatically. This also works across devices (In Chrome it's located at Preferences -> Personal Stuff -> Set up sync)

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Good answer! This is what I would use. :) –  jrg Aug 3 '11 at 18:59
    
Thanks for the suggestion. The idea had occurred to me too and it's probably what I'll end up doing if I want to use Opera often on the second desktop. It's just so frustrating that this is a (possibly) universal problem with browsers but there's nothing in the OS that prevents a program from playing nice with two desktops. Can't you use use sqlite for storage and DBus for messaging ACROSS desktops (if you design your app to use them)? –  Brendan Kidwell Aug 4 '11 at 2:13
    
I think that'd put a lot of strain on the developers, simply because 2-card setups are rather scarce. Have you tried Bumblebee to enable you to use one desktop while switching between both cards? (Perhaps this kind of ruins the purpose of two cards?) –  aureianimus Aug 4 '11 at 5:49
    
I respectfully disagree. As far as I know, all desktop environments (GNOME, KDE, Windows, and OS X) support MULTIPLE logins from different consoles. Lots of apps have no problem with this while keeping often complicated local configuration files/databases. Browsers shouldn't be an exception. Thanks for the suggestion of Bumblebee. Took me a few minutes to figure out what Optimus is, and it looks like my ATI GPUs aren't supported. –  Brendan Kidwell Aug 9 '11 at 3:44
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