Endophytic bacteria can control crop diseases caused by phytopathogenic fungi and promote plant growth, playing an essential role in the development of sustainable agriculture. Herein, 87 endophytic bacteria were isolated from the leaves and roots of soybean plants. The isolate with the strongest inhibition percentage (71.9%) against Macrophomina phaseolina, the causative agent of charcoal rot disease, was genotypically identified as Bacillus pumilus RS11. This strain reduced the severity of damage to seeds and controlled charcoal rot in soybean plants under greenhouse conditions, preserving plant growth parameters and surpassing the efficacy of commercial fungicides. Mass spectrometry–based metabolomics of B. pumilus RS11 monoculture and under coculture conditions with M. phaseolina revealed metabolites with antimicrobial, signalling, and plant growth-promoting activities. Coculture induced the activation of biosynthetic pathways associated with defense metabolites. These findings highlight the multifunctional role of B. pumilus RS11 with potential application as a sustainable bioinput in soybean disease management.