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It is a combination of both. Calibre uses a meta tag to find the cover, as does iTunes and the nook. The Kobo and Sony both use ADE's cover renderer which renders the first page of the ePub. There is one way to create the cover page which will render right for ADE/Sony/Kobo, but Calibre will not mess with the cover page in an ePub if one is already present. It's pretty easy to make a cover page that won't render right. I've got a few I did by hand a couple years ago that are mostly white space, only show the upper left corner of the cover, and one or two with a blank cover.
The way to fix it is explode the ePub and fix the cover page manually. You can also make sure this is your problem by loading the ePub into ADE on your computer and seeing what it shows as the cover.
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