Natural selection, developmental constraint, and plasticity have all been invoked as explanations for intraspecific cranial variation in humans and apes. However, global patterns of human cranial variation are congruent with patterns of genetic variation, demonstrating that population history has influenced cranial variation in humans. Here we show that this finding is not unique to Homo sapiens but is also broadly evident across extant ape species. Specifically, taxa that exhibit greater intraspecific cranial shape variation also exhibit greater genetic diversity at neutral autosomal loci. Thus, cranial shape variation within hominoid taxa reflects the population history of each species. Our results suggest that neutral evolutionary processes such as mutation, gene flow, and genetic drift have played an important role in generating cranial variation within species. These findings are consistent with previous work on human cranial morphology and improve our understanding of the evolutionary processes that generate intraspecific cranial shape diversity within hominoids. This work has implications for the analysis of selective and developmental pressures on the cranium and for interpreting shape variation in fossil hominin crania.