show Abstracthide AbstractHybridization is differentially manifested across the genome, with observed introgression representing a balance between selection and migration. The capacity to quantify introgression and subsequently pinpoint the constituent genetic elements governing cross-species exchange has been promoted by the unprecedented resolution of contemporary sequencing technologies. Furthermore, the availability of annotated reference genomes has allowed genomic patterns to be associated with ecologically relevant phenotypes. We followed this pattern herein by harnessing genomic resources to decipher the role of selection in shaping hybrid zones at the interface of species-boundaries in North American box turtles (Terrapene). By so doing, we identified adaptive divergence in genes related to immune system function and intrinsic thermal adaptations. These, in turn, impact temperature-dependent sex determination and hypoxia tolerance. Their patterns were then contrasted among inter- and intra- specific hybrid zones that differed in a temporal and biogeographic context. Our results demonstrate that hybridization is broadly apparent in Terrapene, but with varying levels of divergence at loci that impinge upon thermal adaptation. These loci displayed signatures of adaptive introgression across intraspecific boundaries, and do so despite a genome-wide selective trend against intergrades. By contrast, interspecific comparisons at the same loci retained evidence of divergence. Importantly, adaptations that shape species-boundaries in Terrapene not only underscore climatic boundaries for these terrestrial ectotherms, but also bookmark their vulnerability to anthropogenic pressures.