Abstract Transposable elements and other repeats are repressed by small‐RNA‐guided histone modifications in fungi, plants and animals. The specificity of silencing is achieved through base‐pairing of small RNAs corresponding to the these genomic loci to nascent noncoding RNAs, which allows the recruitment of histone methyltransferases that methylate histone H3 on lysine 9. Self‐reinforcing feedback loops enhance small RNA production and ensure robust and heritable repression. In the unicellular ciliate Paramecium tetraurelia , small‐RNA‐guided histone modifications lead to the elimination of transposable elements and their remnants, a definitive form of repression. In this organism, germline and somatic functions are separated within two types of nuclei with different genomes. At each sexual cycle, development of the somatic genome is accompanied by the reproducible removal of approximately a third of the germline genome. Instead of recruiting a H3K9 methyltransferase, small RNAs corresponding to eliminated sequences tether Polycomb Repressive Complex 2, which in ciliates has the unique property of catalyzing both lysine 9 and lysine 27 trimethylation of histone H3. These histone modifications that are crucial for the elimination of transposable elements are thought to guide the endonuclease complex, which triggers double‐strand breaks at these specific genomic loci. The comparison between ciliates and other eukaryotes underscores the importance of investigating small‐RNAs‐directed chromatin silencing in a diverse range of organisms. This article is categorized under: Regulatory RNAs/RNAi/Riboswitches > RNAi: Mechanisms of Action