Past climatic fluctuations have heavily influenced species distributions, often causing periods of isolation in refugia, followed by secondary contact and gene flow. Previous mitochondrial analysis of the gray fox (Urocyon cinereoargenteus) identified a division in the Great Plains between eastern and western lineages that were unusually divergent relative to other North American carnivores (up to 1 Mya), possibly representing cryptic species. However, nuclear divergence and reproductive isolation were not investigated. Using both reduced-representation (n = 259) and whole-genome (n = 42) sequencing, we investigated these questions by first assessing divergence time and evidence for admixture, and then, upon discovering an admixture zone, investigating the extent and timing of admixture pulses. Nuclear analyses of divergence supported previous mtDNA estimates of divergence time and indicated a narrow zone of admixture. Using local ancestry reconstruction, we found a recent bi-directional pulse of gene flow that began <100 generations ago, and a more ancient pulse of unidirectional gene flow, from the eastern into the western population, up to ~1,700 generations ago. Based on the estimated ages of these introgression events, we compared the observed cline width to predictions of a null model that assumed neutral introgression and no reproductive barriers. The observed cline width was similar to the predicted cline width, approximately 500 km, providing no clear evidence of reproductive barriers. However, we identified several genomic regions with signatures of selective introgression across the contact zone that were linked previously in other species to olfaction, mate choice, and behavioral divergence.