The remarkable variation of species and phenotypes among insect herbivores is often explained by strong natural selection imposed by plant defenses. While this hypothesis seems to be supported at higher taxonomic levels (e.g. insect families), there is ambiguous evidence at lower taxonomic levels for the effects of plant defenses variation in maintaining insect trait variation and population divergence. I explore the ecological and micro-evolutionary roles of host plant on ecological specialization and population divergence in two co-occurring milkweed herbivores, Rhyssomatus lineaticollis (Say) and R. annectens (Casey). I first asked the questions: is weevil preference and oviposition behavior on two co-occurring milkweed species consistent with ecological specialization? And how is weevil host plant specialization related to species divergence? Through a series of surveys, behavioral assays, and molecular analyses, I found that the two weevil species specialize on a different milkweed species. However, host use patterns were undergoing changes, R. lineaticollis showed clinal variation in oviposition phenotypes and both weevil species seemed to be intermixing. I next investigated if variation in R. lineaticollis oviposition behaviors were a result of phenotypic plasticity or local adaptation to variation in host plant defenses using a common garden experiment. While oviposition behaviors were not plastic in response to host plant genotypes, there was not support for local adaption to plant genotypes. Other environmental or geographic factors may be more relevant for behavioral differences than selection imposed by host plants. Finally, I addressed whether both species were hybridizing and the relative importance of geographic and ecological factors to the weevils’ genetic structure using double digest restriction site associated DNA sequencing (ddRAD-seq) to generate genetic markers within and between species. I confirmed that species divergence is associated with host plant specialization and that a low level of admixture occurs between the species. Concordant with the common garden results, I found that within species genetic structure is more likely linked to selection driven by environmental gradients than to host plant specialization. This work shows that for specialized organisms, ecological and environmental processes can jointly act to generate and maintain population divergence.