AbstractSoil degradation is an ecological disturbance, usually human‐caused, that negatively affects the vegetation and climate of an ecosystem, particularly arid and semiarid environments. These degraded soils can be restored by using native perennial plants inoculated with specific microorganisms. We studied the changes in root growth and the rhizosphere bacterial community of mesquite seedlings (Prosopis articulata) after inoculation with the endophytic bacteria Bacillus pumilus ES4, over 3 cycles of growth in the same soil under desert climatic conditions, and found that inoculation significantly enhanced root biomass during the growth cycles but not shoot biomass or root and shoot lengths. Fluorescent in situ hybridization analysis demonstrated that B. pumilus colonized the root cap, apical meristem, and elongation zone, forming small colonies, on roots from soil‐grown mesquite. Inoculation also significantly changed the bacterial community structure of rhizophere and nonrhizosphere (without plants) soils based on denaturing gradient gel electrophoresis profiles. The changes were highly stable, and the bacterial community structure was maintained throughout the experimental period and not affected by plant replacement. The 16S rRNA pyrosequencing confirmed the changes on structure of bacterial community and revealed an impact on the top taxonomic levels analyzed. The rhizospheres of inoculated plants showed a significant increase in the abundance of Proteobacteria and Acidobacteria coupled with a concomitant decrease in Actinobacteria, whereas an opposite response was observed in nonrhizospheric degraded soils. Overall, inoculation with B. pumilus reduced bacterial diversity but increased the Rhizobium population in the soil. The class Bacilli, despite B. pumilus inoculum, showed minimal variation.