Losing custom #theme settings set in hook_field_widget_form after an error
This one turned out to be a fairly simple fix. I had theme_mymodule_checkboxes living in mymodule.admin.inc which was not being included on every page. Moving the function to the mymodule.field.inc which is specifically included in the module file caused the theme function to be included and fixed the error.

Many thanks to the drupal user Ayalon who found this fix.