Tobacco bacterial wilt (TBW), caused by Ralstonia solanacearum, significantly impacts tobacco yield and quality, leading to substantial economic losses. This study investigated the effects of the microbial agents JX (Pichia sp. J1 and Klebsiella oxytoca ZS4) on the soil properties, rhizospheric microbial community, tobacco agronomic traits, and TBW incidence through field experiments. Our results revealed that JX effectively suppressed TBW (relative control efficiency reached 85.18%) and promoted plant growth, enhancing agronomic traits by 9.58%-49.12%. The microbial agents JX was also attributed to improving soil properties (e.g., organic matter, total nitrogen, total phosphorus, and total potassium). Results of high-throughput sequencing revealed that JX not only affected the structure and diversity of tobacco rhizospheric bacterial/fungal community but also increased the relative abundances of critical microorganisms (e.g., Mesorhizobium, Pedosphaera, Nocardioides, Massilia, Burkholderia, and Purpureocilliu). Functional predictions showed the relative abundance of the pathways about some key secondary metabolisms (e.g., biosynthesis pathway of nicotinamide, phenylpropanoid, indole alkaloids, penicillin, cephalosporin, and novobiocin) and functional enzymes (e.g., catalase, ferroxidase, and tryptophan synthase) increased, which may also be critical factors in promoting tobacco growth and controlling TBW. These findings underscored the effectiveness of JX in both promoting tobacco growth and inhibiting TBW, supporting its practical application in tobacco cultivation.