Each branch of the tree of life includes a myriad of parasitic species but current research does not adequately represent their remarkable diversity. Today, entire parasitic groups have eluded characterization, many with direct impact on human activities. Here, I propose to shed light on one such group, Ascetosporea. This group encloses a large diversity of microbial eukaryote parasites of aquatic invertebrates, including pathogens of shellfish aquacultures, for which we lack even the most fundamental knowledge about their biology. To fill this gap, I aim to provide a comprehensive understanding of the evolution and adaptation to parasitism in this group. We will use new methods to generate de novo genomic data from several species spanning the ascetosporean diversity, as well as close free-living relatives. This information will first be used to establish a strong evolutionary framework for the origin and the relationships among Ascetosporea, using phylogenomics. We will then reveal pre-parasitic conditions, ancestral parasitic innovations, and lineage-specific adaptations, using reconstructed mitochondrial metabolism and comparative genomics. Finally, we will characterize the molecular mechanisms of an ascetosporean infection to identify virulence genes. Altogether, by targeting species that have evolved from an unexplored part of the biosphere, this proposal will improve our understanding of parasitism by allowing comparisons with better-studied model systems.