Understanding species responses to past environmental changes can help forecast how they will cope with ongoing climate changes. Harbor porpoises are widely distributed in the North Atlantic and were deeply impacted by the Pleistocene changes with the split of three subspecies. Despite major impacts of fisheries on natural populations, little is known about population connectivity and dispersal, how they reacted to the Pleistocene changes, and how they will evolve in the future. Here, we used phylogenetics, population genetics, and predictive habitat modeling to investigate population structure and phylogeographic history of the North Atlantic porpoises. A total of 925 porpoises were characterized at 10 microsatellite loci and one quarter of the mitogenome (mtDNA). A highly divergent mtDNA lineage was uncovered in one porpoise off Western Greenland, suggesting that a cryptic group may occur and could belong to a recently discovered mesopelagic ecotype off Greenland. Aside from it and the southern subspecies, spatial genetic variation showed that porpoises from both sides of the North Atlantic form a continuous system belonging to the same subspecies (Phocoena phocoena phocoena). Yet, we identified important departures from random mating and restricted dispersal forming a highly significant isolation by distance (IBD) at both mtDNA and nuclear markers. A ten times stronger IBD at mtDNA compared with nuclear loci supported previous evidence of female philopatry. Together with the lack of spatial trends in genetic diversity, this IBD suggests that migration-drift equilibrium has been reached, erasing any genetic signal of a leading-edge effect that accompanied the predicted recolonization of the northern habitats freed from Pleistocene ice. These results illuminate the processes shaping porpoise population structure and provide a framework for designing conservation strategies and forecasting future population evolution.