Low genomic diversity is generally indicative of small population size and is considered detrimental bydecreasing long-term adaptability. Moreover, small population size may promote gene flow with congeners and outbreeding depression. Here, we examine the connection between habitat availability, effective population size (Ne), and extinction by generating a 40x nuclear genome from the extinct blue antelope (Hippotragus leucophaeus). Historically endemic to the relatively small Cape Floristic Region in southern-most Africa, populations were thought to have expanded and contracted across glacial-interglacial cycles, tracking suitable habitat. However, we found long-term low Ne, unaffected by glacial cycles, suggesting persistence with low genomic diversity for many millennia prior to extinction in AD 1800. A lack of inbreeding, alongside high levels of genetic purging, suggests adaptation to this long-term low Ne and that human impacts during the colonial era (e.g., hunting and landscape transformation), rather than longer-termecological processes, were central to its extinction. Phylogenomic analyses uncovered gene flow between roan (H. equinus) and blue antelope, as well as between roan and sable antelope (H. niger), approximatelyat the time of divergence of blue and sable antelope (1.9 Ma). Finally, we identified the LYST and ASIP genes as candidates for the eponymous bluish pelt color of the blue antelope. Our results revise numerous aspects of our understanding of the interplay between genomic diversity and evolutionary history and provide the resources for uncovering the genetic basis of this extinct species’ unique traits.