In resposne to insect herbivory, plants synthesize and emit blends of volatile compounds from their damaged and undamaged tissues, which act as important host-location cues for parasitic insects. Here we use chemical and behavioural assays to show that these plant emissions can transmit herbivore- specific information that is detectable by parasitic wasps (parasitoids). Tobacco, cotton and maize plants each produce distinct volatile blends in response to damage by two closely related herbivore species, Heliothis virescens and Helicoverpa zea. The specialist parasitic wasp Cardiochiles nigriceps exploits these differences to distinguish infestation by its host, H. virescens, from that by H. zea. The production by phylogenetically diverse plant species and the exploitation by parasitoids of highly specific chemical signals, keyes to individual herbivore species, indicates that the interaction between plants and the natural enemies of the herbivores that attack them is more sophisticated than previously realized.