Common bean root microbiome was used to research for potential biocontrol agents of phytopathogenic fungi as Fusarium sp., Macrophomina sp., and Alternaria sp. causal agents of root rot disease on host plants. Therefore, a bacterial collection of 90 endophytic and rhizospheric isolates was established from field-grown common bean plants in Tunisia and screened for their antifungal activity against pathogenic fungal strains. Antifungal activity was checked at biochemical and genetic levels. Twelve bacterial strains exhibited up to 71% of inhibition of the three pathogenic strains of Fusarium sp., Macrophomina sp., and Alternaria sp. Biocontrol assays conducted under controlled conditions demonstrated that Bacillus amyloliquefaciens, Bacillus halotolerans, Bacillus velezensis, Agrobacterium fabrum, and Pseudomonas lini displayed the highest protective effect on common bean cv. Coco blanc. These bacterial strains were associated with significant plant growth promotion up to 217%, in comparison with control plants. Biochemical analysis of the antagonistic and plant growth promoting activity revealed the production of xylanases, chitinases, siderophore, hydrogen cyanide, phosphate-solubilizing activity, and the production of indole-3-acetic acid, particularly in Bacillus spp. strains. Polymerase chain reaction revealed the presence of lipopeptide biosynthetic genes encoding surfactin, iturin, bacillomycin, and fengycin. The study unveiled that common bean root microbiome contains potential bacterial strains that exhibit efficient biocontrol activity of Fusarium sp., Macrophomina sp., and Alternaria sp., and act as plant growth promoters. Considering various plant growth promoting and biocontrol traits, the study showed the superiority of the Bacillus spp. strains among different common bean root microbiomes.