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Crops are exposed to myriad abiotic and biotic stressors with negative consequences. Two stressors that are expected to increase under climate change are drought and infestation with herbivorous insects, including important aphid species. Expanding our understanding of the impact drought has on the plant–aphid relationship will become increasingly important under future climate scenarios. Here we use a previously characterized plant–aphid system comprising a susceptible variety of barley, a wild relative of barley with partial aphid resistance, and the bird cherry-oat aphid to examine the drought–plant–aphid relationship. We show that drought has a negative effect on plant physiology and aphid fitness, and provide evidence to suggest that plant resistance influences aphid responses to drought stress. Furthermore, we show that the expression of thionin genes, plant defensive compounds that contribute to aphid resistance, increase in susceptible plants exposed to drought stress but remain at constant levels in the partially resistant plant, suggesting that they play an important role in determining the success of aphid populations. This study highlights the role of plant defensive processes in mediating the interactions between the environment, plants, and herbivorous insects. [ABSTRACT FROM AUTHOR]