Oxylipins function as signaling molecules in plant growth and development and contribute to defense against stress. Here, we show that oxylipins also facilitate infestation of Arabidopsis thaliana shoots by the phloem sap-consuming green peach aphid (GPA; Myzus persicae), an agronomically important insect pest. GPAs had difficulty feeding from sieve elements and tapping into the xylem of lipoxygenase5 (lox5) mutant plants defective in LOX activity. These defects in GPA performance in the lox5 mutant were accompanied by reduced water content of GPAs and a smaller population size of GPAs in the mutant compared with the wild-type plant. LOX5 expression was rapidly induced in roots in response to infestation of shoots by GPAs. In parallel, levels of LOX5-derived oxylipins increased in roots and in petiole exudates of GPA-colonized plants. Application of 9-hydroxyoctadecadienoic acid (an oxylipin produced by the LOX5 enzyme) to roots restored water content and GPA population size in lox5 plants, thus confirming that a LOX5-derived oxylipin promotes infestation of the foliage by GPAs. Micrografting experiments demonstrated that GPA performance on foliage is influenced by the LOX5 genotype in roots, thus demonstrating the importance of root-derived oxylipins in colonization of aboveground organs by an insect.