Below-ground herbivory impacts plant development and often induces systemic responses in plants that affect the performance and feeding behavior of above-ground herbivores. Meanwhile, pest-damaged root tissue can enhance a plant's susceptibility to abiotic stress such as salinity. Yet, the extent to which herbivore-induced plant defenses are modulated by such abiotic stress has rarely been studied. In this study, we examine whether root feeding by larvae of the turnip moth, Agrotis segetum (Lepidoptera: Noctuidae) affects the performance of the above-ground, sap-feeding aphid Aphis gossypii (Hemiptera: Aphididae) on cotton, and assess whether those interactions are modulated by salinity stress. In the absence of salinity stress, A. segetum root feeding does not affect A. gossypii development. On the other hand, under intense salinity stress (i.e., 600 mM NaCl), A. segetum root feeding decreases aphid development time by 16.1 % and enhances fecundity by 72.0 %. Transcriptome, metabolome and bioassay trials showed that root feeding and salinity stress jointly trigger the biosynthesis of amino acids in cotton leaves. Specifically, increased titers of valine in leaf tissue relate to an enhanced performance of A. gossypii. Taken together, salinity stress alters the interaction between above- and below-ground feeders by changing amino acid accumulation. Our findings advance our understanding of how plants cope with concurrent biotic and abiotic stressors, and may help tailor plant protection strategies to varying production contexts.