Many species of fungi and oomycetes are plant pathogens of great economic importance. Over the past 7 years, the genomes of more than 30 of these filamentous plant pathogens have been sequenced, revealing remarkable diversity in genome size and architecture. Whereas the genomes of many parasites and bacterial symbionts have been reduced over time, the genomes of several lineages of filamentous plant pathogens have been shaped by repeat-driven expansions. In these lineages, the genes encoding proteins involved in host interactions are frequently polymorphic and reside within repeat-rich regions of the genome. Here, we review the properties of these adaptable genome regions and the mechanisms underlying their plasticity, and we illustrate cases in which genome plasticity has contributed to the emergence of new virulence traits. We also discuss how genome expansions may have had an impact on the co-evolutionary conflict between these filamentous plant pathogens and their hosts.