Conventional RNA interference (RNAi) pathways suppress eukaryotic gene expression at the transcriptional or post-transcriptional level. At the core of RNAi are small RNAs (sRNAs) and effector Argonaute (AGO) proteins. Arabidopsis AGO1 is known to bind microRNAs (miRNAs) and post-transcriptionally repress target genes in the cytoplasm. Here, we report that AGO1 also binds to the chromatin of active genes and promotes their transcription. We show that sRNAs and SWI/SNF complexes associate with nuclear AGO1 and are required for AGO1 binding to chromatin. Moreover, we show that various stimuli, including plant hormones and stresses, specifically trigger AGO1 binding to stimulus-responsive genes. Finally, we show that AGO1 facilitates the induction of genes in jasmonate (JA) signaling pathways and the activation of JA responses. Our findings suggest that, by binding and facilitating the expression of stimuli-specific genes, AGO1 may regulate diverse signaling pathways and associated biological processes.