Shared phylogenetic breaks across taxa, syntopic clusters of endemics, and paleogeographic reconstruction of isostatic and vegetation change over time suggest the existence of one or more ice-free glacial refugia off of North America’s North Pacific Coast. However, both an incomplete fossil record and cosmogenic 10Be exposure dating create uncertainty over whether hypothesized coastal refugia even existed. If refugia existed, then identifying the persistent species is critical to interpretation of the timing, duration, and paleoenvironment-reconstructions. We use whole-genome resequencing to assess the historical biogeography of these complex northern landscapes that span multiple archipelagos and mountain ranges. Unanticipated discovery of genomically-distinct insular and continental clades within forest-associated Pacific martens (M. caurina) is consistent with morphometric and parasitological investigations, and also with the Coastal Refugium Hypothesis. Our results support the persistence of forested refugial communities along the western edges of the Alexander Archipelago. We found no evidence of admixture on islands that received historical translocations of American pine martens (M. americana), but detected introgression in two zones of secondary contact: one insular, one continental. Evidence of early-generational hybrids across multiple hybrid zones, each backcrossed with M. americana, is consistent with a history of genetic dilution of M. caurina through outbreeding. Into the future, these hybrid zones will serve as instructive natural experiments for forecasting outcomes of genetic management initiatives, such as genetic rescue or restoration. Evidence of refugial divergence in a forest-associated, medium-sized carnivore along the North Pacific Coast suggests that genomic reevaluations may identify new perspectives on a suite of forest-associated species and provide new insight into refugial community composition.