Nodules harbour microbial communities composed of rhizobia and other lower-abundance bacteria. These non-rhizobial bacteria can promote plant growth. However, their genomic diversity and how this relates to their plant growth-promoting traits remain poorly investigated. Here, we isolated 14 Pseudomonas strains from the nodules of Lotus plants, sequenced their genomes, analysed their genomic and phylogenetic diversity, and assessed their ability to promote plant growth. We identified five distinct species, including a novel species named Pseudomonas monachiensis sp. nov., with strain PLb12A ^T , as the type strain. Genome analysis of these nodule-isolated Pseudomonas revealed an abundance of genes associated to plant growth-promoting traits, especially auxin-related genes, compared to closely related type strains. In accordance, most nodule-isolated Pseudomonas strains enhanced shoot growth of Lotus burttii, while only some promoted root growth or early onset of root hair proliferation. However, none of the strains significantly affected the ability to form nodules. Overall, our findings highlight the genotypic diversity and the plant growth-promoting potential of nodule-isolated Pseudomonas and underscore their possible applications in mixed inocula with rhizobia.