Asymptomatic plants grown in natural soil are colonized by phylogenetically structured communities of microbes known as the microbiota. Individual microbiota members can activate host innate immunity, which limits pathogen proliferation and curtails plant growth, a phenomenon known as the growth-defense trade-off. We report that in mono-associations, 41% (62/151) of taxonomically diverse root commensals suppress Arabidopsis root growth inhibition (RGI) triggered by immune-stimulating microbe-/damage-associated molecular patterns. 16S rRNA gene amplicon sequencing data reveal that immune activation alters the profile of synthetic communities (SynComs) comprised of RGI non-suppressive strains, while the presence of RGI-suppressive strains attenuates this effect. Chronic root transcriptional outputs in response to colonization with RGI-suppressive or non-suppressive SynComs share a core of genes with a stereotyped expression pattern. However, RGI-suppressive SynComs specifically downregulate a subset of immune-related genes. Such SynCom-specific modulation of defense is physiologically relevant as mutation of one commensal-downregulated transcription factor, MYB15, or pre-colonization with an RGI-suppressive SynCom render plants more susceptible to opportunistic Pseudomonas pathogens. Our results suggest that commensals with contrasting MTI modulating capacities interact with the plant host and together buffer the system against pathogen challenge, defense-associated plant growth inhibition and community shift via a crosstalk with the immune system, leading to commensal-host homeostasis.