In the face of climate change, there is a growing need for research into the ability of organisms to persist at the limits of their bioclimatic envelope. American pikas (Ochotona princeps) have emerged as a focal mammalian species for investigating extinction risk related to climate change; however, most studies have occurred in characteristic alpine talus habitat within the range core. In the Columbia River Gorge (CRG), Oregon, American pikas inhabit low-elevation talus slopes previously considered outside the species' bioclimatic range. We used microsatellite genotypic data to reconstruct levels of genetic variation, population connectivity, and demographic history at 11 CRG sites spanning an elevational gradient (104–1,292 m). Sampled sites separated into 2 genetic clusters largely explained by elevation, topography, and geographic proximity, with pairwise estimates of differentiation and migration rates suggesting little gene flow may be occurring. Sites were characterized by levels of allelic richness and heterozygosity substantially lower than values reported at characteristic alpine sites from the range core. Evidence of recent demographic contraction was found almost exclusively at high-elevation sites despite these areas being considered refuges from climate warming in more typical habitat. Given their unique genetic characteristics and persistence in an atypical environment, the CRG pika populations likely constitute a significant component of intraspecific biodiversity with high conservation value.