Cytosine methylation is one of epigenetic information marked on the DNA sequence. In plants, small interfering RNAs (siRNAs) target homologous genomic DNA sequences for cytosine methylation. This process, known as RNA-directed DNA methylation (RdDM), plays an important role in transposon control, regulation of gene expression and virus resistance. In this paper, we demonstrate that the C2 protein encoded by a geminivirus (beet severe curly top virus, BSCTV) mediated a decrease in DNA methylation of repeat regions in the promoters of ACD6, an upstream regulator of the salicylic acid defense pathway, and GSTF14, an endogenous gene of the glutathione S-transferase superfamily that is implicated in numerous stress responses. C2-mediated decreases in DNA methylation reduced accumulation of the siRNAs derived from the promoter repeats and enhanced the steady-state expression of both ACD6 and GSTF14 transcripts. Reduced accumulation of BSCTV-derived siRNAs was detected in BSCTV-infected plants, but not in plants infected with C2-deficient BSCTV (c2− BSCTV). C2 protein exhibited no siRNA-binding activity. Instead, our results revealed that C2 protein-mediated decreases in DNA methylation appeared to affect the production of siRNAs that are required for targeting and reinforcing RdDM, a process that activated expression of defense-related genes that are normally dampened by these siRNAs in the host plants. However, C2-dependent reduction in virus-derived siRNAs also benefits the viruses by disrupting the feedback loop reinforcing DNA methylation-mediated antiviral silencing.