Soil microbial community changes imposed by the cumulative effects of root-secreted phenolic acids (PAs) promote soil-borne pathogen establishment and invasion under monoculture systems, but the disease-suppressive soil often exhibits less soil-borne pathogens compared with the conducive soil. So far, it remains poorly understood whether soil disease suppressiveness is associated with the alleviated negative effects of PAs, involving microbial degradation. Here, the long-term monoculture particularly shaped the rhizosphere microbial community, for example by the enrichment of beneficial Pseudomonas species in the suppressive soil and thus enhanced disease-suppressive capacity, however this was not observed for the conducive soil. In vitro PA-degradation assays revealed that the antagonistic Pseudomonas species, together with the Xanthomonas and Rhizobium species, significantly increased the efficiency of PA degradation compared to single species, at least partially explaining how the suppressive soil accumulated lower PA levels than the conducive soil. Pot experiments further showed that this consortium harboring the antagonistic Pseudomonas species can not only lower PA accumulation in the 15-year conducive soils, but also confer stronger Fusarium wilt disease suppression compared with a single inoculum with the antagonistic bacteria. Our findings demonstrated that understanding microbial community functions, beyond the single direct antagonism, facilitated the construction of active consortia for preventing soil-borne pathogens under intensive monoculture.