Starships form a recently discovered superfamily of giant transposons in Pezizomycotina fungi, implicated in mediating horizontal transfer of diverse cargo genes between fungal genomes. Their elusive nature has long obscured their significance, and their impact on genome evolution remains poorly understood. Here, we reveal a surprising abundance and diversity of Starships in the phytopathogenic fungus Verticillium dahliae. Remarkably, Starships dominate the plastic genomic compartments involved in host colonization, are enriched in virulence-associated genes, and exhibit genetic and epigenetic characteristics associated with adaptive genome evolution. We further uncover extensive horizontal transfer of Starships between Verticillium species and, strikingly, from distantly related Fusarium fungi. Finally, we demonstrate how Starship activity facilitated the de novo formation of a novel virulence gene. Our findings illuminate the profound influence of Starship dynamics on fungal genome evolution and the development of virulence. ### Competing Interest Statement The authors have declared no competing interest.