SUMMARY Small RNA-mediated RNA silencing is an important antiviral mechanism in higher plants. It has been shown that RNA silencing components can be upregulated by viral infection. However, the mechanisms underlying the upregulation remain largely unknown. Here, we show that JA signaling transcriptionally activates AGO18, a core RNA silencing component that promotes rice antiviral defense through sequestering miR168 and miR528. The JA-responsive transcription factor JAMYB directly binds the AGO18 promoter to activate AGO18 transcription. RSV coat protein (CP) is the elicitor that triggers JA accumulation and upregulates JAMYB. Our study reveals a novel crosstalk between the JA signaling and antiviral RNA silencing and elucidates a molecular mechanism for CP-mediated resistance in monocot crops.