Distinguishing between hybrid zones formed by secondary contact versus parapatric divergence-with-gene-flow is an important challenge for understanding the interplay of geographic isolation and local adaptation in the origin of species. Similarly, distinguishing between natural hybrid zones and those that formed as a consequence of recent human activities has important conservation implications. Recent work has demonstrated the existence of a narrow hybrid zone between the plains gartersnake (Thamnophis radix) and Butler’s gartersnake (T. butleri) in the Great Lakes region of North America, raising questions about the history and conservation value of genetically admixed populations. Both taxa are of conservation concern, and it is not clear whether to regard hybridization as a threat or a natural interaction. Here we use phylogeographic and population genetic methods to assess the timescales of divergence and hybridization, and test for evidence that the hybrid zone is of recent origin. We assayed AFLP markers and ND2 mitochondrial DNA (mtDNA) sequences from T. radix, T. butleri, and the closely related short-headed gartersnake (T. brachystoma) throughout their North American ranges. We find shallow mtDNA divergence overall and high levels of variation within the contact zone. These patterns are inconsistent with recent contact of long-diverged taxa. It is not possible to distinguish true divergence-with-gene-flow from a long-term secondary contact zone, but we infer that the hybrid zone is a long-standing, natural interaction.