Transposable Elements (TEs) have been considered for long as “junk” DNA in the genome of complex eukaryotes. However, massive sequencing efforts coupled with phylogenetic analyses suggest TEs can act as genome shapers and be a source of gene innovation and genome plasticity, eventually contributing to genome divergence. Fungi are simple and easy to manipulate eukaryote organisms, for which the ever-growing genome information indicates that many plant-associated fungi have a tendency towards genome size expansion. This increase in genome size is mostly driven by TE expansion that eventually shapes adaptive regions of the genome. Such genome regions host genes involved in niche adaptation and favor accelerated evolutionary dynamics of these genes. Focusing on the Leptosphaeria maculans-Leptosphaeria biglobosa species complex of closely related plant pathogenic fungi, I will discuss the link between TE invasion/TE bursts in genomes and (i) speciation, (ii) the rise of two-speed genomes, shaping plastic genome environments, (iii) gene diversification that contributed to adaptation to new hosts, (iv) heterochromatinebased regulation of expression of effector genes, (v) accelerated adaptation to resistance gene pressure in gene-forgene systems.