Intense microbial competition in soil has driven the evolution of resistance mechanisms, yet the implications of such evolution on plant health remain unclear. Our study explored the conversion from antagonism to coexistence between Bacillus velezensis ( Bv ) and Trichoderma guizhouense ( Tg ) and its effects on Fusarium wilt disease (FWD) control. We found a bacilysin transmembrane transporter ( Tg MFS4) in Tg , critical during cross-kingdom dialogue with B v. Deleting Tgmfs4 (Δ Tgmfs4 ) mitigated Bv - Tg antagonism, reduced bacilysin import into Tg , and elevated its level in the coculture environment. This increase acted as a feedback regulator, limiting overproduction and enhancing Bv biomass. Δ Tgmfs4 coinoculation with Bv demonstrated enhanced FWD control relative to wild-type Tg ( Tg -WT). In addition, the Tg -WT+ Bv consortium up-regulated antimycotic secretion pathways, whereas the Δ Tgmfs4 + Bv consortium enriched the CAZyme (carbohydrate-active enzyme) family gene expression in the rhizosphere, potentiating plant immune responses. This study elucidates the intricacies of bacterial-fungal interactions and their ramifications for plant health.