Honeydew is a sugar-rich food source produced by sap-feeding insects, notably by major pests such as aphids and whiteflies. It is an important alternative food source for the adult stage of various key natural enemies (e.g., parasitoids), but it may be used also as food by agricultural pests. Necremnus tutae is an idiobiont parasitoid, and it is the most abundant larval parasitoid associated with the South American tomato pinworm, Tuta absoluta, in recently invaded European areas. The impact of N. tutae on T. absoluta populations was evaluated under greenhouse conditions with and without the presence of a honeydew producer, the aphid Macrosiphum euphorbiae. In addition, laboratory experiments were performed to evaluate the longevity of N. tutae and T. absoluta adults when fed with water, honey or honeydew produced by the aphid. In the greenhouse, N. tutae effectively reduced T. absoluta population by the end of the experiment, and this independently of the presence of the aphid; still the presence of M. euphorbiae led to delayed and reduced T. absoluta population peak when controlled by the parasitoid (there was a fourfold increase in parasitoid density in presence of aphid). The longevity of both N. tutae and T. absoluta females increased in the presence of honeydew (when compared to water only) under laboratory conditions; it hinted that honeydew could be used by an herbivore as T. absoluta. The interactions between the two phytophagous species showed contrasting effects, and this mostly independently of parasitoid presence. Tuta absoluta had no impact on aphid population dynamics. By contrast, the production of T. absoluta larvae was higher in the first part of the experiment as the adults lived longer (feeding on aphid honeydew) and produced more larvae. In the second part of the experiment, there were fewer T. absoluta larvae in the presence of the aphid, likely owing to resource competition and/or negative plant-mediated indirect interactions. We demonstrated that honeydew producers could impact parasitoid-host population dynamics both through direct and indirect interactions and that potential positive effects of a sugar food source toward a pest can be nullified in the long term by other negative effects occurring simultaneously.