Sequences affiliated to Syndiniales (Marine alveolate, MALV) regularly dominate 18S rDNA genetic libraries of nearly all marine ecosystems investigated so far. Among them, Amoebophryidae (MALV group II) is composed of numerous and genetically distant environmental sequences, where Amoebophrya is the only known and formally described genus. Amoebophrya species include virulent pathogens for a wide range of dinoflagellate species. Beside their regular occurrence in marine ecosystems, their quantitative distribution and the environmental factors triggering host infection have barely been studied in open oligotrophic waters. In order to understand the functional role of these parasites in natural environments, we studied the distribution and contribution to the eukaryotic community of the small free-living stage of Amoebophryidae (the dinospores) along a transect in the Mediterranean Sea, as well as their host diversity at three oligotrophic stations. Dinospores were more abundant at a coastal station (max. 1.5 × 103 cells ml−1) than in oligotrophic waters (max. 51 ± 16.3 cells ml−1), where they represented 10.3 to 34.9% of the total eukaryotic community at 40 and 30 m depth, respectively and 21.2% on average along the water column. Positive correlation was found between dinospore occurrence and higher concentration of NO3 + NO2 at the coastal station. At selected stations, out of 38 different dinoflagellates taxa identified, 15 were infected, among which a majority were not recognized as Amoebophryidae host so far. Prevalences (percentage of infected cells) generally varied between 1% and 10%, with a notable exception for Blepharocysta paulsenii for which 25% of cells were infected at the most oligotrophic station. The present study shows that dinospores are able to thrive and infect dinoflagellates both in coastal and ultra-oligotrophic open waters. Our results emphasize the role of parasitism in microbial food web dynamics and ultimately on biogeochemical cycles.