Species of the Chytridiomycota, also known as chytrids, belong to a basal lineage in the fungal kingdom inhabiting terrestrial and aquatic environments. Most of the described chytrids are free-living saprophytes, but several species cause important diseases. Examples are Batrachochytrium dendrobatidis responsible for the world wide amphibian decline and Synchytrium endobioticum the causal agent of potato wart disease. Synchytrium endobioticum has an obligate biotrophic lifestyle and isolates can be differentiated based on their virulence on a differential set of potato cultivars, referred to as pathotypes. Quarantine measures have been implemented worldwide to control the disease and to prevent its spread. To determine taxonomical relationships, and to gain insights into the evolution and recent history of introductions of this plant pathogen we assembled and annotated the complete mitochondrial genome of S. endobioticum and generated mitochondrial genomes for five additional chytrid species. The mitochondrial genome of S. endobioticum pathotype 1(D1) strain MB42 is a linear 72,865 bp molecule with terminal inverted repeats that encodes 14 core genes typically found on fungal mitochondrial genomes. Based on single nucleotide polymorphisms the 30 S. endobioticum isolates sequenced could be clustered in four distinct mitochondrial lineages, indicating multiple introductions of the pest to the European main land. These lineages comprise different pathotypes suggesting that pathotypes 2(G1) and 6(O1) have emerged at least twice independently. Variations for polymorphic sites within a strain were observed demonstrating that S. endobioticum strains represent in fact a community of different genotypes. Such a community was shown to be complex and stable over time, but we also demonstrate that the population may shift rapidly based on selection for virulence on a specific R gene from the host.