Understanding how and why species evolve often requires knowledge of intraspecific divergence. In this study, we examine intraspecific divergence in the endangered hot spring snake Thermophis baileyi, an endemic species of the Qinghai-Tibet Plateau. Genomic analyses using a hybrid assembly strategy resulted in a revised, high-quality genome. Whole-genome re-sequencing of 31 sampled individuals from 15 sites served to identify drivers of intraspecific divergence, and explore the potential role gene selection plays in divergence. Our analyses resolved three groups, with inter-group admixture occurring in regions of contact. Divergence seems to have occurred during the Pleistocene because of glacial climatic oscillations and geomorphological changes. Highly diverged regions (HDRs) that distinguish the groups most likely owe to gene sorting. Inter-group HDRs involve genes under positive selection that putatively relate functionally to ecological divergence, and especially reproduction. Our findings reveal the need to integrate multiple aspects to distinguish evolutionary processes potentially involved in speciation.