Hybridization and genetic introgression during the speciation process are now believed to be widespread among many animal groups. Extensive hybrid zones and hybrid introgression in Hyalophora are interpreted in relation to these species and speciation concepts. Historical and current evolutionary studies of Hyalophora, and consequent taxonomic revisions, are reviewed. We emphasize those named (e.g., H. “kasloensis”) and unnamed taxa and populations of apparent hybrid origin. A COI phylogenetic analysis of the genus is presented. Hyalophora cecropia shows minimal haplotype divergence over its distribution and does not form hybrid zones in areas of range overlap with congeners. Hyalophora euryalus also shows minimal genetic divergence despite a large West Coast distribution, where it occupies a diversity of plant communities. By contrast, H. columbia gloveri is subdivided into extensive Great Basin and Rocky Mountain haplotype groups. Hyalophora columbia gloveri is distinguished from H. c. columbia by the smallest haplotype divergence of any inter-taxon comparison. We found a shared haplotype between these subspecies from populations located in the northern Rocky Mountains and Minnesota, respectively. The genetic break between eastern and western H. c. columbia populations mirrors a transition zone seen in morphological and ecological characters that is found in eastern Manitoba and western Ontario. Extensive hybridization occurs wherever H. euryalus and H. c. gloveri overlap, varying from narrow hybrid zones to geographically extensive, self-sustaining populations of exclusively hybrid individuals. Several cases of mitochondrial capture were discovered, in which the predominant haplotype of H. euryalus was incorporated at high frequency in both hybrid populations and populations of phenotypically “pure” H. c. gloveri. Newfound larval and adult phenotypic geographic variation is documented and discussed in terms of a possible origin in hybridization and introgression. Select populations are evaluated as possible examples of hybrid species.