After messing around some more it appears the edited page-template.xpgt file wasn't copying over properly. Now that it did all the margins are 'fixed' except for the right hand one, which appears to be a CSS issue. Unfortunately the CSS for this book is 3,262 lines long so it might take a bit to track it down.
Thanks Jellby for the trouble shooting suggestion
EDIT: Of course right after I posted I found the offending line. Thanks again Jellby.