This turned out to be a pretty straightforward bug with my own code.
The problem was my first form was checking for submission with a simple:
if ( 'POST' == $_SERVER['REQUEST_METHOD'] ) {
so it was being triggered even when the other form was submitted, and my wp_verify_nonce() check would fail and then it would call wp_nonce_ays.
To fix, I added this to the conditional:
and isset( $_POST['sidebar_form_wpnonce'] )
So yes, you can have more than one form/nonce per page.
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