We examined sequence variation in the control region of the mitochondrial genome from 778 seals sampled at 161 locations from northern Japan to southeastern Alaska to learn more about the evolutionary history and population structure of, and effects of recent declines on genetic diversity in, harbor seals (Phoca vitulina) in the northern Pacific Ocean. High haplotypic diversity (H = 0.975) and a poorly resolved mitochondrial genome (mtDNA) phylogeny suggest that harbor seals in the Pacific underwent a rapid expansion in population size in their recent evolutionary past, possibly after the retreat of Pleistocene ice sheets. Weak phylogeographic partitioning of lineages attests to a complex evolutionary and demographic history of contemporary Pacific populations. Extensive macrogeographic subdivision was evident among a subset of grouped localities that represent centers of abundance along the distributional continuum. Heterogeneity was influenced by population size and correlated with geographic distance, suggesting that dispersal occurs primarily among neighboring subpopulations. The 2 currently recognized subspecies of harbor seal in the Pacific, P. v. richardii of North America and P. v. stejnegeri of Asia, do not represent phylogenetically discrete mtDNA assemblages. The greatest differentiation detected was along the Commander–Aleutian Island chain, the region of the presumed subspecies boundary and a likely contact zone for expanding refugial populations of a number of marine mammal species after retreat of ice sheets. Differentiation between the Kodiak Archipelago and Prince William Sound, and between Bristol Bay and the Pribilof Islands, indicates that current management stocks are inappropriate and highlights the need for a detailed analysis of population and stock structure in Alaska. A decline in population size in Prince William Sound over the past few decades was accompanied by a discernible reduction in mtDNA diversity, manifested as a loss of rare haplotypes through random drift. A continued population decline will erode genetic diversity further, with potentially adverse effects on evolutionary potential and individual fitness.