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Fungal pathogens pose escalating challenges to global food security, as resistance has emerged against nearly all major fungicides used in agriculture. RNA-based antifungals offer a sustainable and environmentally friendly alternative for disease control, but their deployment is hindered by RNA instability under environmental conditions, especially in soil. In this study, we engineered two plant-beneficial soil bacteria-Bacillus subtilis (Gram-positive) and Pseudomonas putida (Gram-negative)-to produce double-stranded RNAs (dsRNAs) targeting fungal genes in the foliar and postharvest pathogen Botrytis cinerea and the soilborne pathogen Verticillium dahliae. We found that both bacterial species secrete RNA through extracellular vesicles (EVs) and that these RNAs are transported into fungal cells, demonstrating cross-kingdom RNA trafficking from bacteria to fungi. Application of dsRNA-containing bacterial EVs to plant leaves suppressed B. cinerea infection. In addition, direct treatment with dsRNA-producing bacteria protected both Arabidopsis thaliana and tomato plants from infections by B. cinerea and V. dahliae. Our findings establish beneficial bacteria as a scalable platform for continuous production and delivery of antifungal RNAs, enabling a cost-effective strategy for sustainable crop protection.