Past climatic fluctuations have heavily influenced current species distributions, generating complex evolutionary histories through periods of isolation in refugia as well as secondary contact and gene flow post-expansion. The gray fox (Urocyon cinereoargenteus) represents the most basal extant canid lineage and occurs only in the Americas. Previous mitochondrial analysis identified deeply divergent (up to 1 Mya) eastern and western lineages, and a major phylogeographic break along the Great Plains Suture Zone, indicating that they have been isolated for numerous glacial-interglacial cycles, and may instead represent cryptic species. However, it remains unclear whether these lineages exhibit reproductive isolation, or whether there has been secondary contact and subsequent admixture post-divergence. Using a combination of reduced-representation (n = 259) and whole-genome (n = 42) sequencing, we identified low levels of admixture between eastern and western lineages at the previously described contact zone. Using local ancestry inference, we tested whether the observed admixture was a result of recent vs ancient admixture, and whether there has been a single pulse or multiple pulses of gene flow. Understanding the complexities surrounding the role of climatic refugia on divergence and secondary contact within the gray fox lineage will improve conservation and management of this evolutionarily distinct mesocarnivore.