AbstractMotility and chemotaxis are crucial processes for soil bacteria and plant–microbe interactions. This applies to the symbiotic bacterium Rhizobium leguminosarum, where motility is driven by flagella rotation controlled by two chemotaxis systems, Che1 and Che2. The Che1 cluster is particularly important in free‐living motility prior to the establishment of the symbiosis, with a che1 mutant delayed in nodulation and reduced in nodulation competitiveness. The Che2 system alters bacteroid development and nodule maturation. In this work, we also identified 27 putative chemoreceptors encoded in the R. leguminosarum bv. viciae 3841 genome and characterized its motility in different growth conditions. We describe a metabolism‐based taxis system in rhizobia that acts at high concentrations of dicarboxylates to halt motility independent of chemotaxis. Finally, we show how PTS^Ntr influences cell motility, with PTS^Ntr mutants exhibiting reduced swimming in different media. Motility is restored by the active forms of the PTS^Ntr output regulatory proteins, unphosphorylated ManX and phosphorylated PtsN. Overall, this work shows how rhizobia typify soil bacteria by having a high number of chemoreceptors and highlights the importance of the motility and chemotaxis mechanisms in a free‐living cell in the rhizosphere, and at different stages of the symbiosis.