At high-latitude, climatic shifts hypothetically drove episodes of divergence during isolation in glacial refugia, or ice-free pockets of land that enabled terrestrial species persistence. Upon glacial recession, populations can expand and often come into contact, resulting in admixture between previously isolated groups. To understand how recurrent periods of isolation and contact have impacted evolution at high latitudes, we investigated introgression in the stoat (Mustela erminea), a Holarctic mammalian carnivore, using whole-genome sequences. We identify two temporally isolated introgression events coincident with large-scale climatic shifts: contemporary introgression in a mainland contact zone and ancient contact ~ 200 km south along North America’s North Pacific Coast. Repeated episodes of gene flow highlight the central role of cyclic climates in structuring high-latitude diversity, through refugial divergence and subsequent introgressive hybridization. Introgression followed by allopatry (e.g., insularization) may contribute to expedited divergence of island taxa experiencing substantial glacial flux.