Niche conservatism and niche divergence are both important ecological mechanisms associated with promoting allopatric speciation across geographic barriers. However, the potential for variable responses in widely distributed organisms has not been fully investigated. For allopatric sister lineages, three patterns for the interaction of ecological niche preference and geographic barriers are possible: i) niche conservatism at a physical barrier, ii) niche divergence at a physical barrier, and iii) niche divergence in the absence of a physical barrier. We test for the presence of these patterns in a transcontinentally distributed snake species, the Common Kingsnake (Lampropeltis getula), to determine the relative frequency of niche conservatism or divergence in a single species complex inhabiting multiple distinct niches. We infer the phylogeographic structure of the kingsnake using a rangewide dataset sampled for the mitochondrial gene cyt-b. We use coalescent simulation methods to test for the presence of structured lineage formation versus fragmentation of a widespread ancestor. Finally, we use statistical techniques for creating and evaluating ecological niche models to test for conservatism of ecological niche preferences. Significant geographic structure is present in the kingsnake, for which coalescent tests indicate structured population division. Surprisingly, we find evidence for all three patterns of conservatism and divergence. This suggests that ecological niche preferences may be labile on recent phylogenetic time scales, and that lineage formation in widespread species results from an interaction between inertial tendencies of niche conservatism and natural selection on populations in ecologically divergent habitats.