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Most losses in flax (<i>Linum usitatissimum</i> L.) crops are caused by fungal infections. The new epigenetic approach to improve plant resistance requires broadening the knowledge about the influence of pathogenic and non-pathogenic <i>Fusarium oxysporum</i> strains on changes in the profile of DNA methylation. Two contrasting effects on the levels of methylation in flax have been detected for both types of <i>Fusarium</i> strain infection: Genome-wide hypermethylation and hypomethylation of resistance-related genes (<i>&#946;-1,3-glucanase</i> and <i>chitinase</i>). Despite the differences in methylation profile, the expression of these genes increased. Plants pretreated with the non-pathogenic strain memorize the hypomethylation pattern and then react more efficiently upon pathogen infection. The peak of demethylation correlates with the alteration in gene expression induced by the non-pathogenic strain. In the case of pathogen infection, the expression peak lags behind the gene demethylation. Dynamic changes in tetramer methylation induced by both pathogenic and non-pathogenic <i>Fusarium</i> strains are dependent on the ratio between the level of methyltransferase and demethylase gene expression. Infection with both <i>Fusarium</i> strains suppressed methyltransferase expression and increased the demethylase (<i>demeter</i>) transcript level. The obtained results provide important new information about changes in methylation profile and thus expression regulation of pathogenesis-related genes in the flax plant response to stressors.