Contemporary mammalian biodiversity in North America has been shaped by cycles of population isolation and divergence driven by Quaternary glacial advances, and subsequent expansion and contact during glacial retreats. As a consequence of expansion, divergent lineages from independent refugia came into secondary contact, but the extent to which intermittent admixture contributed to contemporary diversity remains poorly explored. We investigated the role of introgression in genomic evolution of a Holarctic mammal, the ermine (Mustela erminea) using Illumina whole-genome sequence data. We demonstrate divergence among lineages coincident with 4 distinct refugial centers: Beringia, West, East, and North Pacific Coast (NPC). We also identified multiple bouts of hybridization, including contemporary hybridization at a contact zone along the Alaska-Yukon Territory border, between East and Beringian lineages. An independent and earlier episode of admixture suggests East and Beringia lineages previously hybridised to form the NPC Island lineage, a divergent ermine that is consistent with the coastal refugia hypothesis. Isolated in a coastal refuge during the Last Glacial Maximum, the NPC Island lineage subsequently diverged, suggesting a potentially novel model of hybrid speciation: allopatric divergence after ephemeral gene flow, a process that may be more common in high latitude and insular species. While hybrid-based divergence in this coastal environment has immediate evolutionary consequences and conservation implications for ermine, it also offers an alternative lens for viewing the role of islands as engines of biological diversification.