Histone methylation plays important roles in plant development. However, the role of histone methylation in fruit ripening remains unclear. Here, a total of 16 Jumonji domain-containing proteins (JMJs) were identified from banana genome. During fruit ripening, expression of MaJMJ15 was significantly upregulated. Exogenous ethylene accelerated the upregulation whereas 1-methylcyclopropene delayed the process, suggesting that MaJMJ15 positively regulates banana fruit ripening. MaJMJ15 is an H3K27me3 site-specific demethylase. Transient overexpression of MaJMJ15 promoted banana fruit ripening. Moreover, the global H3K27me3 was decreased by MaJMJ15. Furthermore, MaJMJ15 directly targeted several key ripening-related genes (RRGs) in banana including NAC transcription factor 1/2 (MaNAC1/2), 1-aminocyclopropane-1-carboxylate synthase 1 (MaACS1), 1-aminocyclopropane-1-carboxylate oxidase 1 (MaACO1) and expansin 2 (MaEXP2), removed H3K27me3 from their chromatin, and activated their expression. Our data suggest that MaJMJ15 is an H3K27me3 demethylase, which is involved in the regulation of banana fruit ripening by activating expression of key RRGs via removal of H3K27me3.