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Epigenetic modification is important for cellular functions. Trimethylation of histone H3 lysine 4 (H3K4me3), which associates with transcriptional activation, is one of the important epigenetic modifications. In this study, the biological functions of UvKmt2-mediated H3K4me3 modification were characterized in <i>Ustilaginoidea virens</i>, which is the causal agent of the false smut disease, one of the most destructive diseases in rice. Phenotypic analyses of the Δ<i>Uvkmt2</i> mutant revealed that <i>UvKMT2</i> is necessary for growth, conidiation, secondary spore formation, and virulence in <i>U. virens</i>. Immunoblotting and chromatin immunoprecipitation assay followed by sequencing (ChIP-seq) showed that <i>UvKMT2</i> is required for the establishment of H3K4me3, which covers 1729 genes of the genome in <i>U. virens</i>. Further RNA-seq analysis demonstrated that UvKmt2-mediated H3K4me3 acts as an important role in transcriptional activation. In particular, H3K4me3 modification involves in the transcriptional regulation of conidiation-related and pathogenic genes, including two important mitogen-activated protein kinases <i>UvHOG1</i> and <i>UvPMK1</i>. The down-regulation of <i>UvHOG1</i> and <i>UvPMK1</i> genes may be one of the main reasons for the reduced pathogenicity and stresses adaptability of the ∆<i>Uvkmt2</i> mutant. Overall, H3K4me3, established by histone methyltransferase <i>UvKMT2</i>, contributes to fungal development, secondary spore formation, virulence, and various stress responses through transcriptional regulation in <i>U. virens</i>.