Significance The role of herbivore-associated microbes in mediating plant–herbivore interactions has gained recent attention. We show that a parasitoid associated with its caterpillar host not only suppresses the immune system of the caterpillar but also suppresses the induced defenses of the caterpillar’s host plant. Parasitoids inject eggs into their hosts but also inject polydnaviruses that suppress the caterpillar’s immunity. Immunosuppression enables eggs to hatch and develop as larvae within caterpillars. Additionally, the polydnavirus reduces salivary glucose oxidase, the primary elicitor found in the caterpillar’s oral secretions. Caterpillars injected with polydnavirus induce lower plant defenses than untreated caterpillars. Our results reveal a dimension to the complexity of plant–herbivore interactions indicating that polydnaviruses mediate the phenotypes of the parasitoid, herbivore, and plant.