Intake of sugar-rich foods by adult parasitoids is crucial for their reproductive success. Hence, the availability of suitable foods should enhance the efficacy of parasitoids as biological control agents. In situations where nectar is not readily available, homopteran honeydew can be a key alternative food source. We studied the impact of honeydew feeding on the longevity of the larval endoparasitoids Cotesia marginiventris, Campoletis sonorensis and Microplitis rufiventris, all natural enemies of important lepidopteran pests. Females of these wasps lived longer when feeding on honeydew produced by the aphid Rhopalosiphum maidis on barley compared to control females provided with water only. However, they lived shorter than females fed with a sucrose solution. Further investigations with C. marginiventris showed that access to honeydew also increases the number of offspring produced, but less so than access to a sucrose solution. Moreover, it was found that females of this species need to feed several times throughout their life in order to reach optimal longevity and reproductive output. Analyses of the sugars in the honeydew produced by R. maidis on barley revealed that it contains mainly plant-derived sugars, but also several aphid-synthesized sugars. The sugar composition of the honeydew changed as a function of aphid colony size and time a colony had been feeding on a plant. In general, the higher the aphid infestation, the smaller the percentage of aphid-synthesized sugars in the honeydew. Experiments with honeydew sugar mimics allowed us to reject the hypothesis that the relatively poor performance of the parasitoid on a honeydew diet was due to the sugar composition. Instead, the results from additional feeding experiments with diluted honeydew showed that the nutritional value of pure honeydew is primarily restricted by its high viscosity. The possible consequences of these findings for biological pest control are discussed.