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Population dynamics within species at the edge of their distributional range, including the formation of genetic structure during range expansion, are difficult to study when they have had limited time to evolve. Western Fence Lizards (Sceloporus occidentalis) have a patchy distribution at the northern edge of their range around the Puget Sound, Washington, where they almost exclusively occur on imperiled coastal habitats. The entire region was covered by Pleistocene glaciation as recently as 16,000 years ago, suggesting that populations must have colonized these habitats relatively recently. We tested for population differentiation across this landscape using genome-wide SNPs and morphological data. A time-calibrated species tree supports the hypothesis of a post-glacial establishment and subsequent population expansion into the region. Despite a strong signal for fine-scale population genetic structure across the Puget Sound with as many as 8–10 distinct subpopulations supported by the SNP data, there is minimal evidence for morphological differentiation at this same spatiotemporal scale. Historical demographic analyses suggest that populations expanded and diverged across the region as the Cordilleran Ice Sheet receded. Population isolation, lack of dispersal corridors, and strict habitat requirements are the key drivers of population divergence in this system. These same factors may prove detrimental to the future persistence of populations as they cope with increasing shoreline development associated with urbanization.

Divergence is often ephemeral, and populations that diverge in response to regional topographic and climatic factors may not remain reproductively isolated when they come into secondary contact. We investigated the geographical structure and evolutionary history of population divergence withinSceloporus occidentalis(western fence lizard), a habitat generalist with a broad distribution that spans the major biogeographical regions of Western North America. We used double digest RAD sequencing to infer population structure, phylogeny and demography. Population genetic structure is hierarchical and geographically structured with evidence for gene flow between biogeographical regions. Consistent with the isolation–expansion model of divergence during Quaternary glacial–interglacial cycles, gene flow and secondary contact are supported as important processes explaining the demographic histories of populations. Although populations may have diverged as they spread northward in a ring‐like manner around the Sierra Nevada and southern Cascade Ranges, there is strong evidence for gene flow among populations at the northern terminus of the ring. We propose the concept of an “ephemeral ring species” and contrastS. occidentaliswith the classic North American ring species,Ensatina eschscholtzii. Contrary to expectations of lower genetic diversity at northern latitudes following post‐Quaternary‐glaciation expansion, the ephemeral nature of divergence inS. occidentalishas produced centres of high genetic diversity for different reasons in the south (long‐term stability) vs. the north (secondary contact).