In long-lived temperate bats, female philopatry can influence the genetic structure of roosting groups and the potential for individuals to interact across generations. Although direct observation of dispersal between social groups is difficult given the vagility and nocturnal activity of most bats, molecular markers can be used to infer dispersal and mating patterns. Here we report on female philopatry among pallid bats, Antrozous pallidus, a species that exhibits dynamic fission—fusion roosting behavior in which philopatry and familiarity with a roosting area may help individuals choose roost sites and gain benefits associated with social roosting. In addition, we use genetic data to draw inferences about how dispersal and mating relate to the presence of divergent mitochondrial clades, which have been previously reported for pallid bats in western North America. We found significant genetic structure among colonies in central Oregon based on sequence variation at the mitochondrial (mt) DNA control region (pairwise ФФ_ST = 0.08–0.678), but very little structure among colonies for bi-parentally inherited nuclear microsatellites (pairwise F_ST = 0.004–0.01) indicative of female philopatry and male-mediated gene flow. Interestingly, some bats captured in the same colony had mtDNA haplotypes that differed by more than 12% yet failed to exhibit differences at nuclear markers. Thus, even though such divergence values are sometimes associated with species differences, evidence indicates that bats from these clades freely interbreed. This unusual pattern seems likely to be the result of postglacial range expansions from separate southern refugia northwards followed by recent secondary contact.