Plant-herbivore interactions provide well studied examples of coevolution, but little is known about how such interactions are influenced by the third trophic level. Here we show that larvae of the specialized lepidopteran herbivore Heliothis subflexa reduce their vulnerability to natural enemies through adaptation to a remarkable and previously unknown feature of their host plant, Physalis angulata: The fruits of this plant lack linolenic acid (LA), which is required for the development of most insects. By overcoming this nutritional deficiency, H. subflexa larvae achieve numerous advantages. First, they gain near-exclusive access to a food resource: we demonstrate that closely related Heliothis virescens larvae cannot develop on P. angulata fruit unless the fruit are treated with LA. Second, they reduce their vulnerability to enemies: LA is a key component of volicitin, an elicitor of plant-volatile-signaling defenses. We demonstrate that volicitin is absent in the oral secretions of fruit-feeding caterpillars, that the volatile profiles of plants induced by fruit feeding differ from those induced by leaf feeding or by feeding on LA-treated fruit, and that the former are far less attractive to female Cardiochiles nigriceps parasitoids. Finally, they render themselves nutritionally unsuitable as hosts for enemies that require LA for their own development: we show that C. nigriceps larvae fail to develop within the bodies of fruit-feeding caterpillars but do develop in caterpillars feeding on LA-treated fruit. Thus, H. subflexa larvae not only overcome a serious dietary deficiency but also reduce their vulnerability to natural enemies through a form of "biochemical crypsis."