Anthropogenic nitrogen deposition has shifted many ecosystems from nitrogen (N) limitation to phosphorus (P) limitation. Although well documented in plants, no study to date has explored whether N deposition exacerbates P limitation at higher trophic levels, or focused on the effects of induced plant P limitation on trophic interactions. Insect herbivores exhibit strict N : P homeostasis, and should therefore be very sensitive to variations in plant N : P stoichiometry and prone to experiencing deposition-induced P limitation. In the current study, we investigated the effects of N deposition and P availability on a plant-herbivorous insect system. Using common milkweed (Asclepias syriaca) and two of its specialist herbivores, the monarch caterpillar (Danaus plexippus) and milkweed aphid (Aphis asclepiadis) as our study system, we found that experimental N deposition caused P limitation in milkweed plants, but not in either insect species. However, the mechanisms for the lack of P limitation were different for each insect species. The body tissues of A. asclepiadis always exhibited higher N : P ratios than that of the host plant, suggesting that the N demand of this species exceeds P demand, even under high N deposition levels. For D. plexippus, P addition increased the production of latex, which is an important defense negatively affecting D. plexippus growth rate. As a result, we illustrate that P limitation of herbivores is not an inevitable consequence of anthropogenic N deposition in terrestrial systems. Rather, species-specific demands for nutrients and the defensive responses of plants combine to determine the responses of herbivores to P availability under N deposition.