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. An incomplete fossil record, however, creates uncertainty over which species persisted in hypothesized refugia, obscuring interpretation of the timing, potential duration, and surrounding paleoenvironments. We use whole-genome resequencing to assess the historical biogeography of these complex northern landscapes that consist of multiple coastal archipelagos and mountain ranges. Discovery of distinct insular and continental clades within Pacific martens (M. caurina) is consistent with previous morphometric and parasitological studies and also with the Coastal Refugium Hypothesis, thereby supporting the persistence of diverse, potentially forested refugial communities along the western edges of the Alexander Archipelago. We found no evidence of admixture on islands that received translocations of American pine martens (M. americana) in the mid 1900s, but we detected introgression in two geographically distinct zones of secondary contact. 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 with M. americana. Into the future, these hybrid zones will serve as iterative tests for the outcome of admixture, providing instructive natural experiments for forecasting outcomes of proactive measures such as genetic rescue by natural resource managers.