Conserving genetic variation is critical for maintaining the evolutionary potential and viability of a species. Genetic studies seeking to delineate conservation units, however, typically focus on characterizing neutral genetic variation and may not identify populations harboring local adaptations. Here, variation at two major histocompatibility complex (MHC) class II B genes was characterized in four populations of marbled murrelets Brachyramphus marmoratus, a threatened species in which little neutral genetic population structure has been detected. High diversity, as well as evidence of balancing selection, was detected in exon 2 of these genes. Genetic population structure based on MHC markers was uncorrelated to genetic structure estimated with neutral markers, suggesting that selection played a more important role in shaping population structure at these markers than genetic drift. A high proportion of alleles and inferred peptides were unique to a single population, with the Aleutian Islands and southeast Alaska having the highest richness of both. Murrelets sampled in Oregon had low MHC exon 2 allele and inferred peptide richness, and were significantly differentiated from individuals sampled in the Aleutian Islands based on the frequency of exon 2 alleles. In addition, murrelets sampled in Oregon were differentiated from murrelets in both the Aleutian Islands and southeast Alaska based on inferred peptide frequencies, suggesting that the Oregon population could be prioritized for conservation measures. More broadly, combining information from neutral and adaptive genetic markers can improve the delineation of conservation units in threatened species.