Both southwestern white pine and limber pine are threatened by the non-native pathogen Cronartium ribicola that causes the lethal disease white pine blister rust. The morphological traits of the two species across the Southwest are a continuum, and a hybrid zone between the species’ distributions has been suspected for years. Identifying genetic resistance to white pine blister rust in the pines and planting seedlings with those resistance traits are critical components of proactive and restoration strategies to conserve and sustain the species. Essential to this effort is selection of appropriate seed sources, and paramount to that process is understanding which pine species to plant. Utilizing ecological niche modelling, demographic modelling and genomic cline analyses, our results supported an abundance of advanced generation hybrids and a lack of loci exhibiting steep transition in allele frequency across the hybrid zone. Additionally, we found evidence for climate-associated variation in the hybrid index and niche divergence between parental species and the hybrid zone. This research is the first to demonstrate the molecular basis of the hybrid zone and provides valuable insights into the intrinsic and extrinsic (such as climate) factors that facilitate speciation. The location of the hybrid zone assists (spans the R3 and R2 border) restoration planning.