Transposition can impact genome structure and gene expression, resulting in phenotypic changes for selection to act on. Unrestricted transposable element (TE) activity can compromise genomic integrity and decrease population fitness. In eukaryotes, epigenetic modifications, including DNA methylation, help regulate genome stability through repression of TEs. However, the strong repression of TEs could impede the rise of beneficial genetic variation and constrain the evolvability of a biological system. In the case of the wheat fungal pathogen Zymoseptoria tritici, the inactivation of the DNA methyltransferase, Dim2, has resulted in near-complete loss of cytosine DNA methylation associated with an increased transcription of TEs. Interestingly, related species and Z. tritici strains from the pathogen centre of origin still possess an intact copy of the Dim2 gene. We aim to understand whether the loss of TE repression is adaptive and how it affects the evolutionary potential of Z. tritici. We selected eight Z. tritici strains naturally containing an active or inactive dim2 gene copy to generate Dim2 deletion and complementation transformants. By phenotyping the wild-type and mutant lines we have determined that absence of Dim2 and therefore TE silencing, has no immediate effects on Z. tritici fitness. We will now explore if the loss of dim2-dependent TE silencing confers evolutionary advantage in Z. tritici strains by evolving the wild-type and dim2 mutant strains for 52 weeks under optimal or stressful conditions. The genomes of the parental and evolved lines will be sequenced to search for de novo TE variants and their relative frequency will be correlated with the fitness of the evolved lines. The combination of experimental evolution, genomics, and epigenomics will highlight the significance of TE mobility in the evolvability of a wheat pathogen and facilitate further exploration of the role of TEs in the adaptability of organisms to stressful environmental conditions.