The fine-tuned expression dynamics of the effector genes are pivotal for the transition from vegetative growth to host colonization of pathogenic filamentous fungi.  However, mechanisms underlying the dynamic regulation of these genes remain largely unknown.  Here, through comparative transcriptome and chromatin immunoprecipitation sequencing (ChIP-seq) analyses of the methyltransferase PoKmt6 in rice blast fungus Pyricularia oryzae (syn. Magnaporthe oryzae), we found that PoKmt6-mediated H3K27me3 deposition was enriched mainly at fast-evolving regions and contributed to the silencing of a subset of secreted proteins (SP) and transposable element (TE) families during the vegetative growth of P. oryzae.  Intriguingly, we observed that a group of SP genes, which were depleted of H3K27me3 modification, could also be silenced via the H3K27me3-mediated repression of the nearby TEs.  In conclusion, our results indicate that H3K27me3 modification mediated by PoKmt6 regulates the expression of some SP genes in fast-evolving regions through the suppression of nearby TEs.