Commercial harvest severely reduced the abundance of New Zealand fur seals (NZFSs; Arctocephalus australis forsteri), and the subspecies may have become regionally extinct in Western Australia (WA). NZFS populations are now expanding in WA and this study aimed to determine the origin of these populations and distinguish local recruitment from external recolonization. Mitochondrial cytochrome-b gene sequences were obtained from 137 NZFSs from breeding colonies in WA and South Australia (SA), and analyzed with sequences from Tasmania and New Zealand. Genetic differentiation among WA and SA populations was low, indicating extensive genetic exchange throughout this large region. Three unique haplotypes, however, were recorded from WA, supporting the local recruitment hypothesis. Moreover, a test for asymmetrical gene flow identified a predominance of migration from WA to SA, suggesting a role of WA NZFSs in the recovery of more heavily exploited SA NZFS populations. Significant genetic differentiation was evident between SA and Tasmania, indicating limited genetic exchange despite the close proximity of these populations. Examination of our data suggests NZFSs were not extirpated from WA, have retained unique genetic variants, and that peripheral, low-density populations may have had a role in the recolonization of heavily exploited populations.