Germs associated with insect eggs can profoundly mediate interactions between host plants and herbivores, with the potential to coordinate plant physiological reactions with cascading effects on insect fitness. An experimental system was established including the oriental fruit fly (OFF, Bactrocera dorsalis) and tomato to examine the functions of egg-associated germs in mediating plant–herbivore interactions. OFF feeding resulted in significantly increased tannins, flavonoids, amino acids, and salicylic acid in the host tomato. These defensive responses of tomato were induced by the egg-associated germs, including Lactococcus sp., Brevundimonas sp., and Vagococcus sp. Tannins and flavonoids had no significant feedback effects on the pupal weight of OFF, while pupal biomass was significantly decreased by tannins and flavonoids in the germ-free treatment. Metabolome analysis showed that OFF mainly induced metabolic changes in carboxylic acid derivatives. Phenylalanine significantly induced downstream metabolic changes associated with phenylpropanoid accumulation. Finally, we conclude that the effects of egg-associated germs played an important role in facilitating OFF population adaptation and growth by mediating plant defenses, which provides a new paradigm for exploring the interaction of plant–pest and implementing effective pest biocontrol.