The article reviews the role of RNA in epigenetic regulation of gene expression, focusing on small and long non-coding RNAs (lncRNAs). Small RNAs, such as siRNAs and miRNAs, modify chromatin structure and silence transcription by guiding Argonaute-containing complexes to complementary RNA sequences, recruiting histone and DNA methyltransferases. LncRNAs also recruit chromatin-modifying complexes independently of small RNAs, forming co-transcriptional silencing mechanisms. These mechanisms form powerful RNA surveillance systems that detect and silence inappropriate transcription events, providing memory through self-reinforcing epigenetic loops. The review discusses the formation of RNA scaffolds, which are key to these mechanisms. It highlights the role of RNA in heterochromatin assembly, particularly in *Schizosaccharomyces pombe* and *Arabidopsis thaliana*, where small RNAs and histone or DNA methylation events form self-reinforcing epigenetic loops. The article also explores the conservation and divergence of nuclear RNAi pathways in different organisms, including animals, plants, and fungi. Additionally, the review examines the mechanisms by which lncRNAs and mRNAs interact with chromatin-modifying machineries independently of RNAi pathways, such as the recruitment of Polycomb proteins and the targeting of histone methyltransferases. It discusses the role of lncRNAs in dosage compensation, enhancer function, and the silencing of meiotic genes in *S. pombe*. Finally, the article concludes by highlighting the common principles that unify these ancient pathways, emphasizing the recruitment via nascent RNA and the role of RNA in self-reinforcing positive feedback loops. It also raises several important questions about the biogenesis and function of non-coding RNAs that remain to be answered.The article reviews the role of RNA in epigenetic regulation of gene expression, focusing on small and long non-coding RNAs (lncRNAs). Small RNAs, such as siRNAs and miRNAs, modify chromatin structure and silence transcription by guiding Argonaute-containing complexes to complementary RNA sequences, recruiting histone and DNA methyltransferases. LncRNAs also recruit chromatin-modifying complexes independently of small RNAs, forming co-transcriptional silencing mechanisms. These mechanisms form powerful RNA surveillance systems that detect and silence inappropriate transcription events, providing memory through self-reinforcing epigenetic loops. The review discusses the formation of RNA scaffolds, which are key to these mechanisms. It highlights the role of RNA in heterochromatin assembly, particularly in *Schizosaccharomyces pombe* and *Arabidopsis thaliana*, where small RNAs and histone or DNA methylation events form self-reinforcing epigenetic loops. The article also explores the conservation and divergence of nuclear RNAi pathways in different organisms, including animals, plants, and fungi. Additionally, the review examines the mechanisms by which lncRNAs and mRNAs interact with chromatin-modifying machineries independently of RNAi pathways, such as the recruitment of Polycomb proteins and the targeting of histone methyltransferases. It discusses the role of lncRNAs in dosage compensation, enhancer function, and the silencing of meiotic genes in *S. pombe*. Finally, the article concludes by highlighting the common principles that unify these ancient pathways, emphasizing the recruitment via nascent RNA and the role of RNA in self-reinforcing positive feedback loops. It also raises several important questions about the biogenesis and function of non-coding RNAs that remain to be answered.