Invariant Natural Killer T (iNKT) cells recognize lipid antigens presented on CD1d molecules and protect the host against numerous diseases. Transcription factors, such as T-bet and PLZF, participate in iNKT cell development in the thymus, inducing expression of target genes that enable iNKT cells to perform unique effector functions. However, it is unclear how a multitude of transcription factors is orchestrated within an epigenetic framework that controls lineage-specific gene expression. Transcription of lineage-specific genes is regulated by dynamic change of the histone methylation state. In particular, enzymatic removal of methyl groups by the H3K27-specific demethylases UTX and JMJD3 facilitates gene transcription. While widely studied in stem cell biology, little is known about this epigenetic regulation in leukocyte development. Here, we find that H3K27-specific demethylases are essential cell-intrinsic factors for iNKT cell development. UTX-deficient iNKT cells exhibit impaired expression of iNKT signature genes, including NK cell receptors and the transcription factor Tbx21. Genome-wide epigenetic profiling uncovers a decrease in activation-associated H3K4me3 and a reciprocal increase in repressive H3K27me3 marks within the promoters of genes that are downregulated in UTX-deficient iNKT cells. UTX binds to these promoters and its enzymatic demethylase activity is vital for establishing the iNKT gene expression program. Moreover, we identify the AP-1 transcription factor JunB as novel master regulator of the iNKT cell gene signature, highlighted by its molecular interaction with UTX. In addition, we discovered that iNKT cells harbor super-enhancers for their key transcription factors T-bet, PLZF, and JunB, underlining their role in lineage specification. Taken together, we propose a dual mode of action in which UTX binds to the promoters of hallmark genes and in parallel interacts with key iNKT cell transcription factors to regulate gene expression. These findings have profound implications for our understanding how T cell development is controlled by sophisticated epigenetic mechanisms.