Sap-feeding insects of the order Hemiptera, such as aphids, whiteflies and leafhoppers, use stylets to navigate to the plant vascular system for long-term feeding. We previously demonstrated that aphids deposit the effector Mp10 into the cytoplasm of mesophyll cells. Mp10 belongs to a family of chemosensory proteins (CSPs) commonly present in arthropods. In aphids Mp10 is also known as CSP4. How CSPs regulate cellular processes in plants, and in eukaryotic cells in general, is largely unknown. We found that Mp10 suppresses PTI in response to a variety of elicitor molecules, including aphid-derived elicitors. Mp10 interacts with conserved plant target proteins that have key roles in the trafficking and stabilization of membrane proteins, in agreement with our data showing that Mp10 inhibits ROS and Ca2+ bursts to flg22 and promotes the degradation and cellular trafficking of the pattern recognition receptor FLS2. Mining of available genome-sequence data revealed that Mp10 belongs to a clade shared with homologues from other plant-feeding hemipterans, and Mp10 orthologues from other sap-feeders share PTI-suppressive functions and interactions with plant targets. Thus, CSPs in the Mp10 clade may have evolved to suppress PTI in plants early in the evolution of plant-feeding hemipterans. Given that aphids deposit Mp10 in cells upon probing, this effector appears to act as a local anesthetic to inhibit plant perception of aphid feeding.