Holocene-era range expansions are relevant to understanding how a species might respond to the warming and drying climates of today. The harsh conditions of North American deserts have phylogenetically structured desert bat communities but differences in flight capabilities are expected to affect their ability to compete, locate, and use habitat in the face of modern climate change. A highly vagile but data-deficient bat species, the spotted bat (Euderma maculatum), is thought to have expanded its range from central Mexico to western Canada during the Holocene. With specimens spanning this latitudinal extent, we examined historical demography, and used ecological niche modeling (ENM) and phylogeography (mitochondrial DNA), to investigate historic biogeography from the rear to leading edges of the species’ range. The ENM supported the notion that Mexico was largely the Pleistocene-era range, whereas haplotype pattern and Skyline plots indicated that populations expanded from the southwestern US throughout the Holocene. This era provided substantial gains in suitable climate space and likely facilitated access to roosting habitat throughout the US Intermountain West. Incongruent phylogenies among different methods prevented a precise understanding of colonization history. However, isolation at the southern-most margin of the range suggests a population was left behind in Mexico as climate space contracted and are currently of unknown status. The species appears historically suited to follow shifts in climate space but differences in flight behaviors between leading edge and core-range haplogroups suggest range expansions could be influenced by differences in habitat quality or climate (e.g., drought). Although its vagility could facilitate response to environmental change and thereby avoid extinction, anthropogenic pressures at the core range could still threaten the ability for beneficial alleles to expand into the leading edge.