Since the initial discovery of transposable elements (TEs), growing evidence supports their impact on genome evolution, sometimes acting as a driving force for rapid adaptation. Fungi provide unique systems for studying TE-host genome coevolution due to their wide variation in TE coverage, linked to diverse fungal lifestyles, demographic events, and mechanisms regulating transposition. TE activity fosters genetic variability of fungal pathogens directly through insertion within coding or regulatory regions and indirectly by inducing epigenetic modifications. Notably, TE-driven modifications can significantly affect fungal pathogenicity by targeting genes involved in virulence. Our research aims to unravel how the coevolution between transposable elements and host genomes has shaped genome evolution, architecture, and adaptation in fungal pathogens. We concentrate on two extremes: firstly, rust fungi, obligate biotrophic fungal plant pathogens characterized by remarkably large genomes (80Mb-1Gb) with high TE coverage (50-90%); secondly, the hemibiotroph Zymoseptoria species-complex, featuring smaller (40Mb), compartmentalized genomes with lower TE coverage (10-25%). Our approach combines the comprehensive characterization of complete TE repertoires in high-quality reference genomes with transcriptomics, epigenomics, and experimental evolution to explore the dynamics between TE mobility and host-genome regulation mechanisms. Our analyses unveil that genome expansions in rust fungi primarily result from retrotransposon bursts, punctually occurring throughout the evolutionary history of rust fungi. In the Zymoseptoria species-complex, variation in TE mobility correlates with the recent loss of DNA methyltransferase activity and a reduction in Repeat-Induced point mutation (RIP-like) signatures during mitotic proliferation. In shedding light on the different TE dynamics in various fungal pathogen species, we provide new insights into how the different levels of genomic tolerance against TEs reshape eukaryotic genomic landscapes.