The protozoan parasite Haplosporidium costale is known to occur in the USA where it has been associated with sharp seasonal mortality of the Eastern oyster Crassostrea virginica since the 1960’s. In 2019, the parasite was detected for the first time in the Pacific oyster Magallana gigas in France in the context of light mortality and was subsequently detected in archived material collected since 2008. This detection raised several questions regarding the ability of the parasite to maintain in the ecosystem and the potential involvement of other species in its life cycle. To answer these questions, an integrated sampling approach was deployed seasonally in three oyster farming areas where the parasite was already known to occur. Parasite presence was evaluated after checking the presence of PCR inhibitors and using a previously developed and validated Real Time PCR assay, optimized in this study to detect parasite DNA in various environmental compartments. Parasite DNA was almost only detected in cupped oysters. Considering the high number of oysters found positive with low infection intensity, a complementary experiment was undertaken to better characterize sub-clinical infections in oysters. The presence of the parasite was tested twice a week in water and sediment from aquaria hosting cupped oysters from a known infected site. After one month, oysters were sacrificed and tested regarding the presence of the parasite at the tissular level. Altogether, field and experimental results indicate that the parasite is stably established in oyster, particularly in gills, which may act as a reservoir all along the year. The detection of parasite DNA in nanoplankton and sediment suggests that H. costale is released from the oysters outside mortality event. Our results do not support the involvement of other species than cupped oyster in the parasite life cycle except periwinkles, whose role would deserve to be further investigated