Targeted changes in chromatin state at thousands of genes are central to eukaryotic development. RELATIVE OF EARLY FLOWERING 6 (REF6) is a Jumonji-type histone demethylase that counteracts Polycomb repressive complex 2 (PRC2)-mediated gene silencing in plants and was reported to select its binding sites in a direct, sequence-specific manner1-3. Here we show that REF6 and its two close paralogues determine spatial 'boundaries' of the repressive histone H3K27me3 mark in the genome and control the tissue-specific release from PRC2-mediated gene repression. Targeted mutagenesis revealed that these histone demethylases display pleiotropic, redundant functions in plant development, several of which depend on trans factor-mediated recruitment. Thus, Jumonji-type histone demethylases restrict repressive chromatin domains and contribute to tissue-specific gene activation via complementary targeting mechanisms.