Anthropogenic habitat loss and climate change threaten global biodiversity. Effective conservation management requires a detailed understanding of geographic structure, genetic diversity, and demography of threatened species. The black-throated finch, Poephila cincta, is an Australian songbird with two subspecies: atropygialis and cincta. The southern subspecies, cincta, has experienced an ~80% range contraction over the last century and is listed as endangered but genetic surveys of it are incomplete. Here, we use a combination of reduced representation and whole genome sequencing to examine genetic differentiation, spatial genetic structure, and demographic history in both forms of this species. We find that atropygialis and cincta are genetically distinct despite a history of divergence with gene flow and geographically isolated by a biogeographic barrier known as the Einasleigh Uplands. Since they last shared a common ancestor ~400,000 years ago, the two subspecies have experienced distinct demographic trajectories: population expansion in atropygialis and population decline in cincta. We find that the two remnant population centers of cincta, from the Galilee Basin and the Townsville Coastal Plain, each represent genetically distinct lineages that last shared appreciable levels of gene flow ~4,000 years ago. Moreover, we report striking microgeographic genetic structure from the Townsville Coastal Plain between populations <20 km apart associated with barriers to dispersal caused by anthropogenic habitat modification over the last 50 years: namely the construction of the Ross River Dam. Our findings highlight the urgent need for a conservation approach that prioritizes habitat restoration to re-establish population connectivity in the endangered southern black-throated finch.