The non-protein amino acid γ-aminobutyric acid (GABA) has been proposed to be an ancient messenger for cellular communication conserved across kingdoms. GABA has well-defined signalling roles in animals; however, whilst GABA accumulates in plant tissues under stress, and can regulate plant tissue growth, it has not been determined if, how and when GABA acts as an endogenous plant signalling molecule. Here, we establish that endogenous GABA is a bona fide plant signal by demonstrating it antagonises stomatal movements in response to opening and closing stimuli, and modulates plant gas exchange through the direct inhibition of plasma membrane and tonoplast-localised anion transporters within stomatal guard cells. Furthermore, we show that GABA production within guard cells is necessary and sufficient to influence stomatal aperture by restoring drought tolerance to mutant plants with reduced GABA synthesis through stomatal specific genetic complementation, but not through mesophyll-specific complementation. We show that GABA control of stomatal movement is widely conserved across plant families including valuable dicot and monocot crops. Our findings demonstrate that GABA is a novel plant stress signalling molecule that acts via a mechanism not found in animals to fine tune plant gas exchange. Furthermore, we propose GABA acts as a memory of drought stress by resetting stomatal opening to a lower level the day following a reduction in soil water content. These discoveries open novel avenues for manipulating crop water use and tolerance to biotic and abiotic stress.