In cereal cropping systems of the Pacific Northwestern United States (PNW), climate change is projected to increase the frequency of drought during summer months, which could increase water stress for crop plants. Yet, it remains uncertain how interactions between herbivore species are affected by drought stress. Here, interactions between two cereal aphids present in PNW cereal systems, Metopolophium festucae (Theobald) subsp. cerealium (a newly invasive species) and Rhopalosiphum padi L. (a naturalized species), were tested relative to wheat water stress. When aphids were confined in leaf cages on wheat, asymmetrical facilitation occurred; per capita fecundity of R. padi was increased by 46% when M. festucae cerealium was also present, compared to when only R. padi was present. Imposed water stress did not influence this interaction. When aphids were confined on whole wheat plants, asymmetrical competition occurred; cocolonization inhibited M. festucae cerealium population growth but did not affect R. padi population growth. Under conditions of plant water stress, however, the inhibitory effect of R. padi on M. festucae cerealium was not observed. We conclude that beneficial effects of cocolonization on R. padi are due to a localized plant response to M. festucae cerealium feeding, and that cocolonization of plants is likely to suppress M. festucae cerealium populations under ample water conditions, but not when plants are water stressed. This suggests that plant responses to water stress alter the outcome of competition between herbivore species, with implications for the structure of pest communities on wheat during periods of drought.