Fusarium head blight (FHB), mainly caused by fungus Fusariumgraminearum, is a devastating wheat disease worldwide, leading to reduced yield production and compromised grain quality due to contamination by mycotoxins, such as deoxynivalenol (DON). Manipulating the specific gene expression in microorganisms through RNA interference (RNAi) presents an opportunity for new-generation double-stranded RNA (dsRNA)-based formulations to combat a large number of plant diseases. Here, we applied both spray-induced gene silencing (SIGS) and host-induced gene silencing (HIGS) to target five virulence-related and DON-synthesized genes in F.graminearum, including protein kinase gene Gpmk1, zinc finger protein gene FgChy1, transcription factor FgSR, DON synthesis gene TRI5and the cell-end marker protein gene FgTeaA, aiming to effectively control FHB in wheat. Direct spraying of individual or combined small interfering RNA (siRNAs) from the fungus showed reduced expression of target genes and suppressed pathogenic symptoms during F.graminearuminfection in wheat leaves, with the combination of all five siRNAs demonstrating superior resistance. Furthermore, we generated transgenic wheat lines expressing chimeric RNAi cassettes targeting these five genes, and two independent lines exhibited strong resistance to FHB and Fusarium crown rot, and the reduced DON accumulation. Notably, the HIGS transgenic lines did not adversely impact plant growth and yield traits. Collectively, our findings support that SIGS and HIGS represent effective strategies targeting key pathogenic genes for bolstering disease resistance in crops.

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