Genomic diversity is a fundamental component of Earth’s total biodiversity, and requires explicit consideration in efforts to conserve biodiversity. To conserve genomic diversity, it is necessary to measure its spatial distribution, and quantify the contribution that any intraspecific evolutionary lineages make to overall genomic diversity. Here, we describe the range-wide population genomic structure of a threatened Australian rodent, the black-footed tree-rat (Mesembriomys gouldii), aiming to provide insight into the timing and extent of population declines across a large region with a dearth of long-term monitoring data. By estimating recent trajectories in effective population sizes at four localities, we confirm widespread population decline across the species’ range, but find that the population in the peri-urban area of the Darwin region has been more stable. Based on current sampling, the Melville Island population made the greatest contribution to overall allelic richness of the species, and the prioritisation analysis suggested that conservation of the Darwin and Cobourg Peninsula populations would be the most cost-effective scenario to retain more than 90% of all alleles. Our results broadly confirm current sub-specific taxonomy, and provide crucial data on the spatial distribution of genomic diversity to help prioritise limited conservation resources. Along with additional sampling and genomic analysis from the far eastern and western edges of the black-footed tree-rat distribution, we suggest a range of conservation and research priorities that could help improve black-footed tree-rat population trajectories at large and fine spatial scales, including the retention and expansion of structurally complex habitat patches.