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In plants, RNA-directed DNA methylation (RdDM)-mediated transcriptional gene silencing (TGS) is a natural antiviral defense against geminiviruses. Several geminiviral proteins have been shown to target the enzymes related to methylcycle or histone modification; however, it remains largely unknown whether and by which mechanism geminiviruses directly inhibit RdDM-mediated TGS. In this study, we show that Cotton Leaf Curl Multan virus (CLCuMuV) V2 directly interacts with NbAGO4 and the L76S mutation in V2 (V2L76S) abolishes such interaction. We further showed that V2, but not V2L76S can suppresses RdDM and TGS. Silencing of NbAGO4 inhibits TGS, reduces viral methylation level and enhances CLCuMuV DNA accumulation. In contrast, the V2L76S substitution mutant attenuates CLCuMuV infection and enhances viral methylation level. These findings reveal that CLCuMuV V2 contributes to viral infection by interaction with NbAGO4 to suppress RdDM-mediated TGS in plants. [ABSTRACT FROM AUTHOR]