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<i>Mycosphaerella graminicola</i> (synonym <i>Zymoseptoria tritici</i>) causes septoria tritici blotch, one of the most common and economically important diseases of wheat worldwide. The finished genome sequence of this ascomycete was at least 17% repetitive, 70% of which was composed of retrotransposons. All copies of a DNA cytosine methyltransferase gene were located in subtelomeres, except for one on chromosome 6 which appeared to represent the original sequence based on synteny with related species. All copies of this gene including the putative original showed signatures of repeat-induced point mutation (RIP), a mechanism in fungi for inactivating transposons. These mutations led to premature stop codons in the gene sequence. A genome-wide methylation assay showed that <i>M. graminicola</i> lacks cytosine methylation, so all copies of the gene including the original appear to be inactivated. In contrast, a single, un-mutated copy of the DNA methyl transferase was present in 11 other species, and those tested all had cytosine methylation, including two close relatives of <i>M. graminicola</i> that are thought to have diverged within the past 10,500 years. Therefore, recent amplification of a single-copy gene appears to have made all copies including the original visible to the RIP machinery, resulting in a loss of cytosine methylation in the genome of <i>M. graminicola</i>. This may be the first example of a previously single-copy gene that has been amplified and rapidly inactivated in a fungus.