The identification of historical, environmental and biological factors influencing metapopulation connectivity is important for informing management policies and for designing conservation areas to protect biodiversity. The brown smooth-hound shark Mustelus henlei is a key component of the Mexican commercial shark fisheries, one of the largest in the world. However, Mexico lacks conservation management policies for this heavily exploited species. We conducted phylogeographic and population genetic analyses using data from mitochondrial and nuclear DNA markers and from oceanographic variables to assess metapopulation connectivity in M. henlei from the Gulf of California and the Pacific coast of Baja California. We report on historical range expansion during the Pleistocene, probably associated with the last stages of formation of the Gulf of California. From a contemporary perspective, there is significant population structure explained by spatial distance (but not by environmental factors), which contrasts with expectations of high dispersal capacity for this shark. Population- and individual-based genetic analyses suggest that both female philopatry and male-biased dispersal impact on metapopulation structure. These results highlight the importance of protecting nursery areas and habitat connectivity for the conservation management of the species. Our study clarifies important biological aspects of the brown smooth-hound shark that have implications for the design of shark management policies and marine protected areas in the Gulf of California, an iconic marine ecosystem of global significance.