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Below is a typical combobox before it is opened (It is next to where it says "Destination Folder"):

Below is what it looks like when it is opened:

I HAAAATE this behaviour. It assumes what I am looking for is more likely to be close in the list to what was there when I opened the combobox (which is never the case by the way). So, it positions the list with the last item underneath the mouse. But that puts the top of the list off-screen, so if the item I am looking for is at the top, I have to move my mouse up to the top to scroll the list down so I can see all of the items in the list before I can pick it. Below is what I want it to look like, right after I open the box:

Now, I can see all items immediately, and I can select the one I want without having to do any awkward scrolling manoeuvres. Incidentally, this is how windows does it. Sometimes, they get it right.
How can I change GTK's settings to make it do that by default?
You're assuming it's a setting. It looks a bit more like a GtkComboBox bug to me. – user1686 – 2014-06-03T11:21:45.840
It's not a bug. It is the behaviour the makers desired. Like I said in the OP, the reason they did it this way was because they thought items close to the one last selected are more likely to be the next item selected. This is never true, though. Typically, all items are equally likely to be selected next. Even though this behaviour is demonstrably a bad idea, if my experience has taught me anything, it will be impossible to convince them otherwise.
Of course, there might not be a setting either. If there isn't one, I would consider that a bug. – enigmaticPhysicist – 2014-06-03T11:30:34.467