Differentiation, often leading to speciation, is common among island populations of birds. However, migratory species tend to differentiate less because increased movements often preclude the extended periods of allopatry thought to be required for speciation. This interaction of isolation and migration–gene flow is a complex issue in evolutionary biology. We examined the genetics of divergence in Northern Saw-whet Owls (Aegolius acadicus), in which a migratory form (A. a. acadicus) occurs during fall migration and winter, but not at other times of the year, in the range of a sedentary, island form (A. a. brooksi) on Haida Gwaii, British Columbia. We used 2,018 base pairs of mtDNA and genomic data from 405 amplified fragment-length polymorphisms to assess the population genetics and evolutionary history of these two subspecies. Both mtDNA and nuclear genomic markers showed significant divergence between these subspecies, and mtDNA gene flow between them was very low (<1 individual generation⁻¹). These subspecies likely diverged in association with the Wisconsin glacial maximum, ∼16,000 yr BP. The refugial history of the region, life-history traits, and the maintenance of lineage integrity despite current contact suggest that this divergence occurred or is maintained through heteropatric differentiation, probably driven by a loss of migratory behavior in brooksi accompanied by local adaptations.