This study screened and validated functional endophytic bacterial strains from pepper roots with antagonistic activity against P. capsici, providing a sustainable microbial biocontrol strategy for safe pepper production. Antagonistic strains against Phytophthora blight were isolated and screened from chili pepper roots and reintroduced to R/S pepper cultivars via root irrigation. High-throughput sequencing and resistance gene expression analysis revealed their impact on bacterial communities in rhizosphere soil, roots, and stems, and their efficacy in Phytophthora plight suppression. Two endophytic bacterial strains isolated from resistant pepper (CM334) roots-P10 (Paenibacillus aurantiacus) and P29 (Bacillus velezensis)-exhibited plant growth-promoting traits (nitrogen fixation, phosphate solubilization, and potassium mobilization) along with significant antagonistic activity against P. capsici. Pot experiments demonstrated that root irrigation with functional strains differentially modified bacterial community composition across ecological niches in both resistant and susceptible pepper cultivars. Compared to P. capsici-only treatment (P), The P10+P. capsici (PP) and P29+P. capsici (BP) treatments significantly increased the relative abundance of Burkholderia-Caballeronia-Paraburkholderia (BCP) by 1.58-37.65 percentage points in rhizosphere soil, roots, and stems. This indicated that BCP, as a core bacterial genus induced by inoculation, played a vital biocontrol role against P. capsici in pepper. Moreover, the functional strains significantly upregulated resistance-related genes (CaPR1 and CaHY5) in pepper roots and enhanced defense enzyme activities (POD, PPO, PAL) in leaves of both susceptible and resistant cultivars. This study obtained two endophytic bacterial strains exhibiting effective antagonism against P. capsici, which provides both theoretical support and potential biocontrol resources for eco-friendly management and safe production of pepper crops.