Marked with high levels of endemism and in situ radiations, the Western Ghats mountains make for a compelling backdrop to examine processes that lead to the formation and maintenance of species. Regional geographic barriers and paleoclimatic fluctuations have been implicated as drivers of speciation, but their roles have not been explicitly tested in a phylogenomic framework. We integrated mitochondrial DNA, genome-wide SNPs and climatic data to examine the influence of geographic barriers and climatic transitions in shaping phylogeography and potential speciation in the Peninsular Indian Flying lizard (Draco dussumieri). We found strong evidence for two independently evolving, geographically distinct, northern and southern lineages within D. dussumieri that diverged during the early Pleistocene, and a gradient of admixed populations across a broad hybrid zone in the Central Western Ghats. Migrations after initial divergence were continuous, but gene flow remained consistently below thresholds required to homogenise lineages. We found more support for isolation by environment (especially rainfall regimes) than by distance. The range-break between lineages occurs at a transition zone in the Central Western Ghats that separates dissimilar rainfall regimes with no physical barriers. This limit is potentially an ecological barrier, which nevertheless was permeable during glacial maxima. We hypothesise that similar phylogeographic patterns will emerge in other widespread, wet-adapted species in the Western Ghats that presumably endured the same climatic processes.