The increased availability of quality genomic data has greatly improved the scope and resolution of our understanding of the recent evolutionary history of wild species adapted to extreme environments and their susceptibility to anthropogenic impacts. The guanaco (Lama guanicoe), the largest wild ungulate in South America, is a good example. The guanaco is well adapted to a wide range of habitats, including the Sechura Desert, the high Andes Mountains to the north, and the extreme temperatures and conditions of Navarino Island to the south. Guanacos also have a long history of overexploitation by humans. To assess the evolutionary impact of these challenging habitats on the genomic diversity, we analyzed 38 genomes (similar to 10 to 16x) throughout their extensive latitudinal distribution from the Sechura and Atacama Desert to southward into Tierra del Fuego Island. These included analyses of patterns of unique differentiation in the north and geographic region further south with admixture among L. g. cacsilensis and L. g. guanicoe. Our findings provide new insights on the divergence of the subspecies similar to 800,000 yr BP and document two divergent demographic trajectories and to the initial expansion of guanaco into the more southern portions of the Atacama Desert. Patagonian guanacos have experienced contemporary reductions in effective population sizes, likely the consequence of anthropogenic impacts. The lowest levels of genetic diversity corresponded to their northern and western limits of distribution and some varying degrees of genetic differentiation. Adaptive genomic diversity was strongly linked with environmental variables and was linked with colonization toward the south followed by adaptation.