Recent years have witnessed renewed interest in defining the embryonic cell populations that directly contribute to the bony skull. This question lies at the intersection of several important developmental, clinical and evolutionary interests. Until recently, our collective understanding of the embryonic origin of the vertebrate osteocranium has been based on a small number of reports published solely using avian models. As data gradually accumulates from other, distantly related species (e.g., mouse and frog), we can begin to evaluate long-standing assumptions regarding the behavior of osteogenic (bone-forming) neural crest cells within a wider phylogenetic and comparative context. In this review, we summarize data collected to date in three major vertebrate taxa: amphibians, birds and mammals. We highlight three largely unexplored topics within the field of osteogenic neural crest development: 1) disagreements in bone tissue origin within and across current model systems; 2) whether the pattern of neural crest cell contribution to skull bone is evolutionarily conservative or labile; and 3) how our understanding of development and morphology will benefit from fate maps using currently unexamined animal models.