Ecologists are increasingly aware of the interplay between evolutionary history and ecological processes in shaping current species interaction patterns. The inclusion of phylogenetic relationships in studies of species interaction networks has shown that closely related species commonly interact with sets of similar species. Notably, the degree of phylogenetic conservatism in antagonistic ecological interactions is frequently stronger among species at lower trophic levels than among those at higher trophic levels. One hypothesis that accounts for this asymmetry is that competition among consumer species promotes resource partitioning and offsets the maintenance of dietary similarity by phylogenetic inertia. Here, we used a regional plant-herbivore network comprised of Asteraceae species and flower-head endophagous insects to evaluate how the strength of phylogenetic conservatism in species interactions differs between the two trophic levels. We also addressed whether the asymmetry in the strength of the phylogenetic signal between plants and animals depends on the overall degree of relatedness among the herbivores. We show that, beyond the previously reported compositional similarity, closely related species also share a greater proportion of counterpart phylogenetic history, both for resource and consumer species. Comparison of the patterns found in the entire network with those found in subnetworks composed of more phylogenetically restricted groups of herbivores provides evidence that resource partitioning occurs mostly at deeper phylogenetic levels, so that a positive phylogenetic signal in antagonist similarity is detectable even between closely related consumers in monophyletic subnetworks. The asymmetry in signal strength between trophic levels is most apparent in the way network modules reflect resource phylogeny, both for the entire network and for subnetworks. Taken together, these results suggest that evolutionary processes, such as phylogenetic conservatism and independent colonization history of the insect groups may be the main forces generating the phylogenetic structure observed in this particular plant–herbivore network system.