Strong balancing selection on the Major Histocompatibility Complex (MHC) can lead to different patterns in gene frequencies and neutral genomic variation within species. We investigated diversity and geographic structure of MHC genes DQA and DQB, as well as their inferred functional haplotypes, from two regional populations (East and West Coast) of the endangered Hector’s dolphin (Cephalorhynchus hectori hectori) and the critically endangered Māui dolphin (Cephalorhynchus hectori maui) (West Coast, North Island), and contrasted these results with patterns from neutral microsatellites. The Māui had the lowest number of alleles for DQA (2) and DQB (3), consistent with strong genetic drift acting on this remnant population. However, the two retained DQA alleles are amongst the most divergent combinations of all four alleles found across the Hector’s metapopulation, potentially reflecting the retention of divergent alleles due to balancing selection. The high frequency of the divergent DQB04 allele also gave this population the highest nucleotide diversity for DQB. Strong differentiation was evident for DQA, DQB, and DQA-DQB haplotypes between the regional populations of Hector’s dolphins (FST>0.213) and both subspecies (FST>0.311). Differentiation was generally greater than observed at neutral microsatellite loci, suggesting the influence of selection between geographically proximate East and West Coast populations. This might be the result of spatial differences in directional selection on those opposite coastlines. Additionally, measures of the ratio of non-synonymous to synonymous substitutions (dN/dS) were consistent with balancing selection over evolutionary time. Together, these results suggest a complex interplay of balancing selection, directional selection, local fidelity, and genetic drift.