Bacterial biocontrol agents that antagonize soilborne pathogens are increasingly considered alternatives to chemical pesticides, but their in vivo efficacy is often inconsistent, restricting commercial use. The efficacy of a biocontrol agent can depend on rhizosphere competence and its interaction with native microbiomes, which can affect ecosystem functioning. This study investigated the capacity of a Bacillus cereus sensu lato biocontrol strain (S-25) to persist on roots and in the rhizosphere of cucumber and evaluated its impact on bacterial and fungal community composition in the rhizosphere in the absence and presence of Rhizoctonia solani, the causative agent of damping-off disease in young seedlings. Following amendment, S-25 abundance in the cucumber rhizosphere decreased by two orders of magnitude but remained relatively high for the duration of the experiment, in contrast to the root surface, where it was not detected. Amendment with S-25 significantly reduced the incidence of disease caused by R. solani without reducing the relative abundance of the fungal pathogen. Interestingly, R. solani did not substantially alter the rhizosphere microbial community, whereas S-25 reduced bacterial diversity and facilitated a shift in community composition, with increased relative abundance of Acidobacteriota and Actinomycetota, and reduced abundance of Pseudomonadota, Bacteroidota, and Verrucomicrobiota. Collectively, this study provides important insights into the mode of persistence of biocontrol agents and their effect on native microbiomes in the rhizosphere of pathogen-inoculated plants. It demonstrates that amendment can significantly alter local microbiomes and suggests that optimizing amendment regimes or selecting strains with higher rhizosphere competence can enhance future biocontrol agents.