Quantifying the craniofacial skeletal phenotype during development highlights potential effects of known mutations on bone maturation and is an informative first step for the analysis of animal models. We introduce a novel technique to easily and efficiently quantify individual cranial bone volume and relative bone mineral density across the murine skull from high resolution computed tomography images. The approach can be combined with existing quantitative morphometric methods to provide details of bone growth and bone quality, which can be used to make inferences about regulatory effects local to individual bones and identify locations and developmental times for which additional analyses are warranted. Analysis of the Fgfr2+/Y394C mouse model of Beare-Stevenson cutis gyrata syndrome, an FGFR-related craniosynostosis syndrome, is used to demonstrate the method. Mutants and unaffected littermates display similar bone volume and relative bone density at birth, followed by significant differences at postnatal day eight. The change in rates of bone volume growth occurs similarly for all bones of the skull, regardless of origin, location or association with craniosynostosis. These results suggest an association between low bone density, low bone volume, and Fgfr craniosynostosis mutations. Our novel technique provides an initial quantitative evaluation of local shifts in bone maturation across the skull of animal models.