SummaryIn plants, the exogenous transgene transcribing inverted‐repeat (exo‐IR) sequences produces double‐stranded RNAs that are processed by DCL4. The 21‐nt small interfering RNAs generated function as mobile signals to trigger non‐cell autonomous silencing of target endogenes in the neighboring 10–15 cells. The potential involvement of nuclear silencing pathway components in signal spreading or sensing in target cells is not clear. Here, we demonstrate that the exo‐IR silencer (exo‐Pdsi) is negatively autoregulated through methylation spreading, which acts in cis to reinforce the self‐silencing of the silencer. Mutations affecting nuclear proteins DRD1 and Pol V (NRPE1 or NRPD2) relieved exo‐Pdsi self‐silencing, resulting in higher levels of Pdsi transcripts, which increased the non‐cell autonomous silencing of endo‐PDS. Our results suggest that in an experimental silencing pathway, methylation spreading on a silencer transgene may not have a direct endogenous plant counterpart when the protein‐encoding gene is the target. DRD1‐Pol V‐dependent de novo methylation, by acting in cis to reinforce self‐silencing of exo‐IR, may play a role in restraining the inappropriate silencing of active protein‐coding genes in plants.