Nautiliniellidae Miura and Laubier, 1989 is a small family of marine polychaetes with 20 currently described species in 11 genera, most of which are known to live symbiotically in the mantle cavity of bivalves, mainly from cold seeps and hydrothermal vents, while Calamyzidae (Hartmann‐Schröder, 1971) including only one described species, Calamyzas amphictenicola Arwidsson 1932 lives as an ectoparasite on ampharetid polychaetes in Swedish waters. Nautiliniellidae and Calamyzidae have both been considered to belong to Phyllodocida, but the few phylogenetic studies including these taxa have found their positions unstable. The internal relationships within Nautiliniellidae are also poorly understood. Using molecular information from both nuclear and mitochondrial genes and morphological data we assessed the systematic placement of Nautiliniellidae (seven species; collected from Pacific hydrothermal vents and cold seeps and one from Atlantic waters) and Calamyzas amphictenicola. Our results show that C. amphictenicola and Nautiliniellidae formed a well‐supported clade that is nested within Chrysopetalidae, a free‐living group of polychaetes. The chrysopetalid genus Vigtorniella Kiseleva 1992; a bacterial mat grazer found at methane seeps, anoxic basins and whalefalls, formed a paraphyletic grade with respect to the Nautiliniellidae–Calamyzas clade. The internal relationships within the Nautiliniellidae–Calamyzas clade as well as the relationships with their hosts are also examined. As a result we synonymize Calamyzidae and Nautiliniellidae with Chrysopetalidae, with the last as the oldest available family‐group name. Within Chrysopetalidae we refer to the subfamilies Chrysopetalinae Ehlers 1864; Dysponetinae Aguado, Nygren & Rouse, herein; and Calamyzinae Hartmann‐Schröder, 1971. Calamyzinae contains C. amphictenicola, all taxa formerly in Nautiliniellidae, and the chrysopetalid genus Vigtorniella.