Polycomb repressive complex 2 (PRC2) is responsible for the trimethylation of lysine 27 of histone H3 (H3K27me3)-mediated transcriptional silencing. At present, its biological roles in the devastating rice pathogenic fungus Ustilaginoidea virens remain unclear. In this study, we analyzed the function of a putative PRC2 catalytic subunit UvKmt6. The results showed that disruption of UvKMT6 resulted in reduced growth, conidiation and pathogenicity in U. virens. Furthermore, UvKmt6 is essential for establishment of H3K27me3 modification, which covers 321 genes in the genome. Deletion of UvKMT6 led to transcriptional derepression of 629 genes, 140 of which were occupied with H3K27me3 modification. Consistent with RNA-seq and ChIP-seq analysis, UvKmt6 was further confirmed to participate in the transcriptional repression of genes encoding effectors and genes associated with secondary metabolites production, such as PKSs, NRPSs and Cytochrome P450s. Notably, we found that UvKmt6 is involved in transcriptional repression of oxidative, osmotic, cell wall and nutrient starvation stresses response-related genes. From the perspective of gene expression and phenotype, in addition to the relatively conservative role in fungal development, virulence and production of secondary metabolites, we further reported that UvKmt6-mdediated H3K27me3 plays a critical role in the response to various stresses in U. virens.