Stygiopontius senokuchiae is a hydrothermal-vent-specific copepod species (Dirivultidae, Siphonostomatoida) and abundantly distributes near vent orifices. This species is thought to have an early juvenile planktic stage, and previous studies using bulk tissue stable-isotope and radioisotope data suggest that adults ingest chemoautotrophic microbes growing on vent chimneys. However, ontogenetic changes in their diets have not been investigated. We analysed gut contents of copepodite I to adult stages of S. senokuchiae collected from a hydrothermal-vent chimney at the Izu-Ogasawara Arc to check for the presence of bacterial cells in oral tubes and guts. We compared these results with an unidentified co-occurring calanoid and a species of Ectinosoma (Harpacticoida) and to other Siphonostomatoid copepods, namely Hatschekia labracis (Hatschekiidae), which was attached to a scarbreast tuskfin (Choerodon azurio, Labridae), and Asterocheres sp. 1 (Asterocheridae), which was attached to a spirastrellid sponge. Carbon isotope ratios of S. senokuchiae at different stages and Ectinosoma were measured to complement the nutritional insights obtained from gut-content analysis. Our results clearly showed that most S. senokuchiae individuals possessed bacteria in the oral tube or gut regardless of growth stage, whereas the coexisting Ectinosoma and calanoid did not. The carbon isotopic compositions confirmed that S. senokuchiae gains its nutrition from chemoautotrophic bacteria that use the rTCA carbon-fixation pathway. Comparisons with other Siphonostomatoida copepods suggest that Dirivultidae are specifically adapted to feed on bacteria at hydrothermal-vent chimneys, allowing their high dominance and evolutionary success in these habitats.