The histone H3K27 demethylase, UTX, is a known component of the H3K4 methyltransferase MLL complex, but its functional association with H3K4 methylation in human cancers remains largely unknown. Here we demonstrate that UTX loss induces epithelial–mesenchymal transition (EMT)‐mediated breast cancer stem cell (CSC) properties by increasing the expression of the SNAIL, ZEB1 and ZEB2 EMT transcription factors (EMT‐TFs) and of the transcriptional repressor CDH1. UTX facilitates the epigenetic silencing of EMT‐TFs by inducing competition between MLL4 and the H3K4 demethylase LSD1. EMT‐TF promoters are occupied by c‐Myc and MLL4, and UTX recognizes these proteins, interrupting their transcriptional activation function. UTX decreases H3K4me2 and H3 acetylation at these promoters by forming a transcriptional repressive complex with LSD1, HDAC1 and DNMT1. Taken together, our findings indicate that UTX is a prominent tumour suppressor that functions as a negative regulator of EMT‐induced CSC‐like properties by epigenetically repressing EMT‐TFs.