In understanding the impact of commercial whaling, it is important to estimate the mixing of low latitude breeding populations on Antarctic feeding grounds, particularly the endangered humpback whale populations of Oceania. This paper estimates the degree of genetic differentiation among the putative populations of Oceania (New Caledonia, Tonga, the Cook Islands and French Polynesia) and Australia (western Australia and eastern Australia) using ten microsatellite loci and mtDNA, assesses the power of the data for a mixed-stock analysis, determines ways to improve statistical power for future studies and estimates the population composition of Antarctic samples collected in 2010 south of New Zealand and eastern Australia. A large proportion of individuals could not be assigned to a population of origin (> 52%) using a posterior probability threshold of > 0.90. The mixed-stock analysis simulations however, produced accurate results with humpback whales reapportioned to their population of origin above the 90% threshold for western Australia, New Caledonia and Oceania grouped using a combined mtDNA and microsatellite dataset. Removing the Cook Islands, considered a transient region for humpback whales, from the simulation analysis increased the ability to reapportion Tonga from 86% to 89% and French Polynesia from 89% to 92%. Breeding ground sample size was found to be a factor influencing the accuracy of population reapportionment whereas increasing the mixture or feeding ground sample size improved the precision of results. The mixed-stock analysis of our Antarctic samples revealed substantial contributions from both eastern Australia (53.2%, 6.8% SE) and New Caledonia (43.7%, 5.5% SE) [with Oceania contributing 46.8% (5.9% SE)] but not western Australia. Despite the need for more samples to improve estimates of population allocation, our study strengthens the emerging genetic and non-genetic evidence that Antarctic waters south of New Zealand and eastern Australia are used by humpback whales from both eastern Australia and the more vulnerable breeding population of New Caledonia, representing Oceania.