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The climate-driven acceleration of forest disease outbreaks has intensified the demand for sustainable biocontrol strategies. In this study, we evaluated the effects of the endophytic bacterium Bacillus amyloliquefaciens csuftcsp75 on soil properties, microbial communities, and functional metabolism in soils affected by Pinus massoniana shoot blight. Soil physicochemical analysis, carbon substrate utilization profiling (AWCD), and diversity indices (the Shannon, Simpson, and McIntosh indices) were integrated to assess the microbial responses under different inoculation treatments. The csuftcsp75 treatment significantly improved soil nutrient availability—especially available phosphorus and potassium—and was associated with enhanced microbial metabolic activity and sustained functional diversity. Principal component analysis and correlation mapping revealed strong associations between labile nutrients and microbial responses. Comparative analysis showed that csuftcsp75 promoted a balanced and metabolically rich microbial community, while less compatible strains exhibited transient or unstable effects. These findings support a dual-pathway model wherein nutrient-driven metabolic activation and ecological integration jointly determine biocontrol efficacy. This study highlights the importance of matching microbial inoculants with local soil environments to optimize functional outcomes. This work provides a theoretical basis for applying endophytic Bacillus in forest disease management and contributes to the development of ecologically coherent biocontrol strategies. Full article