To assess effects of historical climate change on northern species, we quantified the population history of the arctic ground squirrel (Spermophilus parryii), an arctic-adapted rodent that evolved in Beringia and was strongly influenced by climatic oscillations of the Quaternary. Competing hypotheses for the species’ population history were derived from patterns of mitochondrial (mtDNA) structure and a bioclimatic envelope model (BEM). Hypotheses invoked (1) sequential isolation of regional populations beginning with the Arctic, (2) deep isolation only across central Alaska, and (3) widespread panmixia, and were tested using coalescent methods applied to eight nuclear (nDNA) loci. The data rejected strict interpretations of all three hypotheses, but perspectives underlying each encompassed aspects of the species’ history. Concordance between mtDNA and nDNA geographic structure revealed three semi-independently evolving phylogroups, whereas signatures of gene flow at nDNA loci were consistent with a historical contact between certain populations as inferred by the BEM. Demographic growth was inferred for all regions despite expectations of postglacial habitat contraction for parts of Beringia. Our results highlight the complementary perspectives on species’ histories that multiple lines of evidence provide, and underscore the utility of multilocus data for resolving complex population histories relevant to understanding effects of climate change.