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Major prehistoric forces, such as the climatic shifts of the Pleistocene, can remain visible in a species’ population genetics. Inference of refuges via genetic tools is useful for conservation management as it can identify populations whose preservation may help retain a species’ adaptive potential. Such investigation is needed for Australia’s southern hairy-nosed wombat (Lasiorhinus latifrons), whose conservation status has recently deteriorated, and whose phylogeographic history during the Pleistocene may be atypical compared to other species. Its contemporary range spans approximately 2000 km of diverse habitat on either side of the Spencer Gulf, which was a land bridge during periods of Pleistocene aridity that may have allowed for migration circumventing the arid Eyrean barrier. We sampled from animals in nearly all known sites within the species’ current distribution, mainly using non-invasive methods, and employed nuclear and mitochondrial DNA analyses to assess alternative scenarios for Pleistocene impacts on population structure. We found evidence for mildly differentiated populations at the range extremes on either side of Spencer Gulf, with secondary contact between locations neighbouring each side of the barrier. These extreme western and eastern regions, and four other regions in between, were genetically distinct in genotypic clustering analyses. Estimates indicate modest, but complex gene flow patterns among some of these regions, in some cases possibly restricted for several thousand years. Prior to this study there was little information to aid risk assessment and prioritization of conservation interventions facilitating gene flow among populations of this species. The contributions of this study to that issue are outlined.