Background: Nematodes are an important component of deep-sea hydrothermal vent communities, but only few nematode species are able to cope to the harsh conditions of the most active vent sites. The genus Oncholaimus is known to tolerate extreme geothermal conditions and high sulphide concentrations in shallow water hydrothermal vents, but it was only occasionally reported in deep-sea vents. In this study, we performed morphological, genetic and ecological investigations (including feeding strategies) on an abundant species of Oncholaimus recently discovered at Lucky strike vent field on the Mid-Atlantic Ridge at 1700 m water depth. Results: We described this species as Oncholaimus dyvae sp. nov.. This new species differs from all other members of the genus by the combination of the following characters: body length (up to 9 mm), the presence of a long spicule (79 mu m) with a distally pointed end, a complex pericloacal setal ornamentation with one precloacal papilla surrounded by short spines, and a body cuticule with very fine striation shortly posterior to the amphid opening. Overall, O. dyvae sp. nov. abundance increased with increasing temperature and vent emissions. Carbon isotopic ratios suggest that this species could consume both thiotroph and methanotrophic producers. Furthermore sulfur-oxidizing bacteria related to Epsilonproteobacteria and Gammaproteobacteria were detected in the cuticle, in the digestive cavity and in the intestine of O. dyvae sp. nov. suggesting a potential symbiotic association. Conclusions: This study improves our understanding of vent biology and ecology, revealing a new nematode species able to adapt and be very abundant in active vent areas due to their association with chemosynthetic micro-organisms. Faced by the rapid increase of anthropogenic pressure to access mineral resources in the deep sea, hydrothermal vents are particularly susceptible to be impacted by exploitation of seafloor massive sulfide deposits. It is necessary to document and understand vent species able to flourish in these peculiar ecosystems.