Pythium spp. poses a serious threat to agricultural production worldwide, but its severity is often neglected because little knowledge about it is available. Using an ITS amplicon metagenomics approach, we investigated the occurrence, abundance, and diversity of Pythium spp. in 127 corn fields of 11 European countries over three years. As a result, we identified 69 Pythium species, with up to 19 species in a single soil sample. We identified also highly prevalent and distributed species in most countries, with significant genetic diversity and varying disease potential, demonstrating a dynamic sharpening process of Pythium communities in Europe corn fields. Infection experiments with isolated isolates indicate that Pythium species differ strongly in their infection progression and disease potential, where an effective interference with plant hormone networks to suppress JA (jasmonate)-mediated defenses seems to be a crucial part of the virulence mechanism of pathogenic Pythium species. This study provides for the first time a valuable data set to gain deep insights into the structural and genetic diversity of Pythium communities in European corn fields and to better understand plant-Pythium interactions and, in particular, the evolution of virulence and pathogenicity, thus facilitating the development of an effective strategy to cope with this pathogen.