Plant growth-promoting bacteria (PGPRs) have the potential to act as biofertilizers and biopesticides. This study was planned to explore indigenously isolated PGPRs as a potential candidate to control charcoal rot that affects various crops including soybean. Among the four different tested species of PGPRs, Bradyrhizobium japonicum (FCBP-SB-406) showed significant potential to enhance growth and control soil borne pathogens such as Macrophomina phaseolina. Bacillus subtilis (FCBP-SB-324) followed next. Bradyrhizobium japonicum (FCBP-SB-406) reduced disease severity up to 81.25% in comparison to the control. The strain showed a strong fertilizing effect as a highly significant increase in biomass and other agronomic parameters was recorded in plants grown in its presence. The same was supported by the Pearson's correlation and principal component analysis. A decrease in disease incidence and severity may be due to the induced resistance imparted by the bacterium. This resulted in significant increments in quantities of defense enzymes, including catalase, peroxidase (PO), polyphenol oxidase (PPO), phenylalanine ammonia lyase (PAL) and superoxide dismutase (SOD). A significant production of proteases, catalases and hydrogen cyanide by B. japonicum (FCBP-SB-406) can also be associated to mycoparasitism. The establishment of PGPRs in treated soils also showed positive effects on soil health. Total metabolite profiling of treated plants in comparison to the control showed the upregulation of many flavonoids, isoflavonoids and amino acids. Many of these compounds have been well reported with antimicrobial activities. Bradyrhizobium japonicum (FCBP-SB-406) can be employed for the production of a potential formulation to support sustainable agriculture by reducing the input of synthetic pesticides and fertilizers.