Plant performance depends on the soil microbiome. While microbiome feedbacks are well documented, the mechanisms by which plants perceive and mediate these feedbacks remain unclear. We established a framework using two distinct microbiomes in the same soil, where one led to enhanced growth of the Arabidopsis thaliana accession Col-0. Screening 410 accessions revealed substantial variation in growth feedbacks, which we used for genome-wide association mapping. We identified the immune receptor Mediator of Microbiome Feedback 1 (MMF1) as a candidate gene involved in microbiota feedbacks. Characterisation in the reference accession Col-0 revealed that mmf1 mutants lost the beneficial growth feedback, had an altered root bacterial community, and failed to induce a defence-related transcriptional response observed in wild-type plants. The discovery of MMF1 implies that integration of microbial signals optimises host microbiome composition and immune status to enhance growth.