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During the last 2 centuries, southern right whales Eubalaena australis were hunted to near extinction, and an estimated 150 000 were killed by pre-industrial whaling in the 19th century and illegal Soviet whaling in the 20th century. Here we focus on the coastal calving grounds of Australia and New Zealand (NZ), where previous work suggests 2 genetically distinct stocks of southern right whales are recovering. Historical migration patterns and spatially variable patterns of recovery suggest each of these stocks are subdivided into 2 stocks: (1) NZ, comprising NZ subantarctic (NZSA) and mainland NZ (MNZ) stocks; and (2) Australia, comprising southwest and southeast stocks. We expand upon previous work to investigate population subdivision by analysing over 1000 samples collected at 6 locations across NZ and Australia, although sample sizes were small from some locations. Mitochondrial DNA (mtDNA) control region haplotypes (500 bp) and microsatellite genotypes (13 loci) were used to identify 707 individual whales and to test for genetic differentiation. For the first time, we documented the movement of 7 individual whales between the NZSA and MNZ based on the matching of multilocus genotypes. Given the current and historical evidence, we hypothesise that individuals from the NZ subantarctic are slowly recolonising MNZ, where a former calving ground was extirpated. We also suggest that southeast Australian right whales represent a remnant stock, distinct from the southwest Australian stock, based on significant differentiation in mtDNA haplotype frequencies (FST = 0.15, p < 0.01; ΦST = 0.12, p = 0.02) and contrasting patterns of recovery. In comparison with significant differences in mtDNA haplotype frequencies found between the 3 proposed stocks (overall FST = 0.07, ΦST = 0.12, p < 0.001), we found no significant differentiation in microsatellite loci (overall FST = 0.004, G’ST = 0.019, p = 0.07), suggesting ongoing or recent historical reproductive interchange.