1. An herbivore's life‐history strategy, including optimization of resource use, is constrained by its evolutionary history and ecological factors varying across the landscape.
2. We asked if related and co‐distributed herbivore species maintain consistency of host preference and oviposition behaviours along the species' range. We surveyed two putative species of milkweed stem weevils, Rhyssomatus lineaticollis and R. annectens, which co‐occur alongside their hosts, Asclepias syriaca and A. incarnata.
3. We confirmed the two species status of weevils, supported by differences in morphology and a bilocus gene phylogeny. Furthermore, we found that species divergence recapitulated the weevils current host plant use.
4. We found oviposition variation within and between species. R. annectens poked the stem haphazardly or girdled it before oviposition. Meanwhile, R. lineaticollis primarily trenched stems in the north, but poked or girdled in the south. Variation in oviposition patterns could be a response to variation in host plant defenses.
5. In nature, weevils strictly oviposited on their respective host plants, while in bioassays, R. lineaticollis exhibited strong preference for A. syriaca and R. annectens fed equally on both host plants.
6. Overall, our results support that milkweed stem weevils are strict specialists but might be undergoing changes in host use. R. lineaticollis specializes on A. syriaca but has two distinct modes of oviposition. Meanwhile R. annectens seems to be more accepting of other hosts. We hypothesize that these weevils might be shifting host use associated with changes in host plant distributions.