To examine how genetic variation in a plant population affects arthropod community richness and composition, we quantified the arthropod communities on a synthetic population of Eucalyptus amygdalina, E. risdonii, and their F1 and advanced‐generation hybrids. Five major patterns emerged. First, the pure species and hybrid populations supported significantly different communities. Second, species richness was significantly greatest on hybrids (F1 > F2 > E. amygdalina > E. risdonii). These results are similar to those from a wild population of the same species and represent the first case in which both synthetic and wild population studies confirm a genetic component to community structure. Hybrids also acted as centers of biodiversity by accumulating both the common and specialist taxa of both parental species (100% in the wild and 80% in the synthetic population). Third, species richness was significantly greater on F1s than the single F2 family, suggesting that the increased insect abundance on hybrids may not be caused by the breakup of coadapted gene complexes. Fourth, specialist arthropod taxa were most likely to show a dominance response to F1 hybrids, whereas generalist taxa exhibited a susceptible response. Fifth, in an analysis of 31 leaf terpenoids that are thought to play a role in plant defense, hybrids were generally intermediate to the parental chemotypes. Within the single F2 family, we found significant associations between the communities of individual trees and five individual oil components, including oil yield, demonstrating that there is a genetic effect on plant defensive chemistry that, in turn, may affect community structure. These studies argue that hybridization has important community‐level consequences and that the genetic variation present in hybrid zones can be used to explore the genetic‐based mechanisms that structure communities.