Root nodules of legume plants are primarily inhabited by rhizobial nitrogen-fixing bacteria. Here we propose two new Rhizobiales species isolated from root nodules of common sainfoin (Onobrychis viciifolia), as shown by core-gene phylogeny, overall genome relatedness indices and pan-genome analysis.Mesorhizobium onobrychidis sp. nov., actively induces nodules, and achieves atmospheric nitrogen and carbon dioxide fixation. This species appears to be depleted in motility genes, and is enriched in genes for direct effects on plant growth performance. Its genome reveals functional and plant growth-promoting signatures like a large unique chromosomal genomic island with high density of symbiotic genetic traits. Onobrychidicola muellerharveyae gen. nov. sp. nov., is described as type species of the new genus Onobrychidicola in Rhizobiaceae. This species comprises unique genetic features and plant growth-promoting traits (PGPTs), which strongly indicate its function in biotic stress reduction and motility. We applied a newly developed bioinformatics approach for in silico prediction of PGPTs (PGPT-Pred), which supports the different lifestyles of the two new species and the plant growth-promoting performance of M. onobrychidis in the greenhouse trial.