The ability of plants to perceive and react to biotic and abiotic stresses is critical for their health. We recently identified a core set of genes consistently induced by members of the leaf microbiota, termed general non-self response (GNSR) genes. Here we show that GNSR components conversely impact leaf microbiota composition. Specific strains that benefited from this altered assembly triggered strong plant responses, suggesting that the GNSR is a dynamic system that modulates colonization by certain strains. Examination of the GNSR to live and inactivated bacteria revealed that bacterial abundance, cellular composition and exposure time collectively determine the extent of the host response. We link the GNSR to pattern-triggered immunity, as diverse microbe- or danger-associated molecular patterns cause dynamic GNSR gene expression. Our findings suggest that the GNSR is the result of a dose-responsive perception and signalling system that feeds back to the leaf microbiota and contributes to the intricate balance of plant-microbiome interactions.