The last Pleistocene deglaciation shaped temperate and boreal communities in North America. Rapid northward expansion into high latitudes created distinctive spatial genetic patterns within species that include closely related groups of populations that are now widely spread across latitudes, while longitudinally adjacent populations, especially those near the southern periphery, often are distinctive due to long-term disjunction. Across a spatial expanse that includes both recently colonized and long-occupied regions, we analyzed molecular variation in zapodid rodents to explore how past climate shifts influenced diversification in this group. By combining molecular analyses with species distribution modeling and tests of ecological interchangeability, we show that the lineage including the Preble's meadow jumping mouse (Zapus hudsonius preblei), a US federally listed taxon of conservation concern, is not restricted to the southern Rocky Mountains. Rather, populations along the Front Range are part of a single lineage that is ecologically indistinct and extends to the far north. Of the 21 lineages identified, this Northern lineage has the largest geographic range and low measures of intra-lineage genetic differentiation, consistent with recent northward expansion. Comprehensive sampling combined with coalescent-based analyses and niche modeling lead to a radically different view of geographic structure within jumping mice and indicates the need to re-evaluate their taxonomy and management. This analysis highlights a premise in conservation biology, that biogeographic history should play a central role in establishing conservation priorities.