Climate change inevitably leaves behind a genetic footprint within phylogeographic legacies of affected species, as individuals are driven to either disperse to track suitable conditions or adapt in situ. One potential consequence is the possibility of hybridization among species, as both geographic ranges and adaptive landscapes shift. The admixture resulting from these newly formed 'contact zones' has various outcomes, to include the creation of new lineages. Interpreting these within the context of historic climate change provides clues necessary to predict biotic responses (and thus evolutionary trajectories) as a function of contemporary shifts. Herein, we dissect historic contact zones for Massasaugas (Viperidae; Sistrurus spp.) within two distinct North American regions (southwestern United States and Central Great Plains) using ddRAD sequencing. We identified fine-scale but previously unrecognized population structure within the southwestern contact zone, where we detected contemporary intergradation between Prairie and Desert massasaugas (S. tergeminus tergeminus, and S. t. edwardsii, respectively), with primary divergence indicated by demographic model selection. Within the Central Great Plains, we found evidence for historic secondary contact via Quaternary climatic cycles, subsequently followed by range expansion at the suture zone separating S. tergeminus and S. catenatus. Extant Missouri populations represent ancestral/relictual vestiges of this earlier hybridization, isolated between the eastern terminus of S. t. tergeminus and the western edge of S. catenatus. Our results illustrate how abrupt climate change has driven ancestral hybridization, cryptic diversity, and range dynamism within Sistrurus.