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Coleogyne ramosissima Torr. (blackbrush) is a dominant xerophytic shrub species in the ecotone between the warm and cold deserts of interior western North America. Amplified fragment length polymorphisms (AFLPs) were used to survey genetic diversity and population genetic structure at 14 collection sites across the species range. Analysis revealed significant population differentiation (F-ST = 0.103, p < 0.0001) and reasonably high levels of genetic diversity (expected heterozygosity; H-E = 0.26), a surprising result for a putative paleoendemic species. Model-based Bayesian clustering, principal coordinates analysis, and neighbor-joining analysis all produced support for the existence of two metapopulations, the first centered on the Mojave Desert and the second on the Colorado Plateau. These genetic data, coupled with information from Late Pleistocene and Holocene packrat (genus Neotoma Say and Ord, 1825) middens, illustrate a demographic history in which eastern and western distributions were disjunct during the Last Glacial Maximum and remained so through the Holocene, forming the present-day metapopulations in the Mojave Desert and Colorado Plateau. This strong regional genetic differentiation has implications for population persistence and migration in response to future climate change, as well as for shrubland restoration following anthropogenic disturbances such as annual grass invasion and wildfire.