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It's quite possible the algorithm used to load in cover images for display has issues once you exceed some numerical threshold (whether the images are from Amazon or anywhere else). Kindle system resources are relatively limited, so there are always trade-offs between performance and stability.
Also possible that there are certain calibre-generated cover images that the thumbnail algorithm has problems with. I've seen a number of discussions where it seemed they had to be of specific dimensions, or thumbnails would not get generated and that sort of thing.
But knowing there is a problem doesn't necessarily give way to some simple solution. It could take considerable effort to isolate the origin of the problem. And you could be getting some reading in instead.
If you were to raise the issue with the right people in Amazon Customer Support, they could pull logs off of your Kindle and probably ascertain something about why it is happening. That doesn't necessarily mean a solution would be forthcoming from their side, of course, but in my experience they do try. The calibre forums here might also be a good place to ask about this.
Short of that, the advice I would take away would be to use Cover View more sparingly. "Doctor, it hurts when I do THIS" "Then don't do THAT".
In general, I almost always find it a lot quicker to use Search to find things in my library. A few keystrokes is usually sufficient.
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