Harnessing the plant microbiome through plant genetics is of increasing interest to those seeking to improve plant nutrition and health. While genome‐wide association studies (GWAS) have been conducted to identify plant genes driving the plant microbiome, more multidisciplinary studies are required to assess the relationships among plant genetics, plant microbiome and plant fitness. Using a metabarcoding approach, we characterized the rhizosphere bacterial communities of a core collection of 155 Medicago truncatula genotypes along with the plant phenotype and investigated the plant genetic effects through GWAS. The different genotypes within the M. truncatula core collection showed contrasting growth and nutritional strategies but few loci were associated with these ecophysiological traits. To go further, we described its associated rhizosphere bacterial communities, dominated by Proteobacteria, Actinobacteria and Bacteroidetes, and defined a core rhizosphere bacterial community. Next, the occurrences of bacterial candidates predicting plant ecophysiological traits of interest were identified using random forest analyses. Some of them were heritable and plant loci were identified, pinpointing genes related to response to hormone stimulus, systemic acquired resistance, response to stress, nutrient starvation or transport, and root development. Together, these results suggest that plant genetics can affect plant growth and nutritional strategies by harnessing keystone bacteria in a well‐connected interaction network.