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. Display omitted •AGO1 binds to the chromatin of transcribed genes•AGO1 binding to chromatin requires small RNAs and SWI/SNF•AGO1 promotes the transcription of AGO1-bound genes•Hormone and stress stimuli trigger AGO1 binding to stimulus-responsive genes Argonaute (AGO) proteins are well known to bind small RNAs and direct post-transcriptional gene silencing. Liu et al. uncover an unsuspected role for Arabidopsis AGO1 in direct chromatin binding to promote gene transcription in responses to stimuli, including hormones and stresses. AGO1 binding requires small RNAs and the SWI/SNF chromatin-remodeling complexes.