Systemin, the first signalling peptide identified in plants, mediates induced resistance against insect herbivores and necrotrophic pathogens in tomato(1-3). Initially, systemin was conceived as a hormone-like, long-distance messenger that triggers systemic defence responses far from the site of insect attack. It was later found to rather act as a phytocytokine, amplifying the local wound response for the production of downstream signals that activate defence gene expression in distant tissues(4). Systemin perception and signalling rely on the systemin receptor SYR1(5). However, the specifics of SYR1-dependent signalling and how systemin signalling differs from other immune signalling pathways remain largely unknown. Here we report that systemin activates the poltergeist-like phosphatase PLL2 in a SYR1-dependent manner. PLL2, in turn, regulates early systemin responses at the plasma membrane, including the rapid inhibition of proton pumps through dephosphorylation of their regulatory C-termini. PLL2 was found to be essential for downstream defence gene induction, ultimately contributing to insect resistance.