It is generally considered that Polycomb Repressive Complex (PRC)2 deposits the histone mark H3K27me3 on silent protein-coding genes, while transposable elements are repressed by DNA and/or H3K9 methylation. Yet, there is increasing evidence that PRC2 also targets and even silences transposable elements in representatives of several distantly related eukaryotic lineages. In plants and animals, H3K27me3 is present on transposable elements in mutants and specific cell types devoid of DNA methylation. In this Opinion, we summarize the experimental evidence for this phenomenon across the eukaryotic kingdom, and discuss its functional and evolutionary significance. We hypothesize that an ancestral role of Polycomb group (PcG) proteins was to silence transposable elements. It has been generally accepted that H3K9me2-3/DNA methylation and H3K27me3 silent heterochromatin marks are found in mutually exclusive genomic regions and display distinct properties.This view is challenged by recent observations of transposable elements marked by H3K27me3.We hypothesize an ancestral association of H3K27me3 with silencing of transposable elements. As multicellular eukaryotes evolved, H3K27me3 became associated with gene silencing, while H3K9/DNA methylation became dedicated to silencing transposable elements.