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Abstract The North American racers (Coluber constrictor) are widely distributed across the Nearctic and numerous studies have demonstrated extensive variation in morphology, ecology, and population genetic structure. Here we take an integrative approach to understand lineage diversification within this taxon by combining genomic sequence capture data, mtDNA sequence data, morphometrics, and ecological niche models. Both the genomic data and mtDNA phylogeographic analyses support five lineages distributed across the range of this species. However, demographic model selection based on these two datasets strongly conflict in both the model of divergence and estimates of timing of lineage divergence. While mtDNA and concatenated genomic data suggest a Miocene origin of these distinct groups, coalescent-based demographic models with the sequence capture data suggest lineage diversification occurred at ~33 kya in allopatry without gene flow. Using linear morphological measurements of head shape we demonstrate that lineages distributed largely east and west of the Mississippi River are distinguishable. Furthermore, ecological niche models demonstrate that lineages distributed in subtropical habitats have environmental niche space that is significantly differentiated from lineages distributed across the continent. Taken together, these results suggest that ecology is an important axis of lineage divergence within this group and that more fine-scale analyses may find even greater differentiation between the populations identified here. This abstract translated to Spanish is avaliable in the Supporting Infromation section (Este resumen traducido al español está disponible en la sección, Supporting Infromation).