In many fungal phytopathogens, infection is regulated by accessory genomic regions enriched in facultative heterochromatin, but the precise role of this chromatin state in virulence is poorly understood. Here we examined the two facultative heterochromatic marks H3K27me and H3K36me in the tomato-pathogenic Fusarium oxysporum isolate Fol 4287, by genetically analyzing the corresponding histone methyltransferases Kmt6 and Ash1. Fol has three KMT6 homologs, two of which, KMTB/C, are encoded on an accessory chromosome. Loss of the core gene KMT6A resulted in strongly reduced but not abolished H3K27me, revealing that methylation of subtelomeres can be taken over by the accessory copy Kmt6b. To the best of our knowledge, this demonstrates for the first time that accessory fungal histone modifiers can contribute to the overall epigenetic profile. Deletion of KMT6A or ASH1 resulted in derepression of in planta-induced effector genes under axenic conditions. KMT6A deletion mutants were blocked at early stages of root infection and were non-pathogenic on tomato plants, but were still able to kill the animal host Galleria mellonella. Constitutive overexpression of the pathogenicity-related transcription factor FTF1 in the ∆kmt6a background restored effector gene activation in planta but not pathogenicity, suggesting that additional facultative heterochromatin-regulated virulence factors are essential for plant infection.