The tortricid moth genus Syndemis has ten described species, with two polyphagous species in Europe and North America respectively. We sequenced five nuclear and four mitochondrial genes for Syndemis samples across both continents and discovered unexpected, extensive diversification restricted to California. DNA evidence supports five new, undescribed, species endemic to California, while the rest of North America and Europe have only one species each. Further, the nuclear genes are less variable and yield contrasting phylogenetic signal compared to mitochondrial DNA for basal relationships between taxa across the genus. Such conflict strongly suggests that male and female moths exhibit radically different levels of philopatry. Our results highlight the importance of sex-specific behavior, and the need for inclusion of multiple genes to fully understand species boundaries, their causes, and the process of speciation. While mtDNA introgression often is invoked to explain incongruous haplotype distributions, our study shows that nuclear DNA selective sweeps, or swamping, can occur while mtDNA and ecology preserve an ancient divergence that is not discernable in nuclear DNA. This study further demonstrates that diversification of herbivores may occur on relictual, declining hostplants, which contrasts with the dominant co-speciation model.