AbstractThe community structure in the plant-associated microbiome depends collectively on host–microbe, microbe–microbe and host–microbe–microbe interactions. The ensemble of interactions between the host and microbial consortia may lead to outcomes that are not easily predicted from pairwise interactions. Plant–microbe–microbe interactions are important to plant health but could depend on both host and microbe strain variation. Here we study interactions between groups of naturally co-existing commensal and pathogenic Pseudomonas strains in the Arabidopsis thaliana phyllosphere. We find that commensal Pseudomonas prompt a host response that leads to selective inhibition of a specific pathogenic lineage, resulting in plant protection. The extent of protection depends on plant genotype, supporting that these effects are host-mediated. Strain-specific effects are also demonstrated by one individual Pseudomonas isolate eluding the plant protection provided by commensals. Our work highlights how within-species genetic differences in both hosts and microbes can affect host–microbe–microbe dynamics.