A new genus of ectoparasitic marine annelids living on ctenophores, Ctenophoricola gen. nov., is described and its feeding behaviour, reproduction and developmental stages are discussed. Its unusual morphology challenged its placement within the known marine families. However, analyses of mitochondrial and nuclear sequence data showed the new genus as member of the Alciopini, a group of holopelagic annelids included within the Phyllodocidae. Ctenophoricola masanorii sp. nov. from Japan and Ctenophoricola rousei sp. nov. from the Canary Islands (Spain) are described. A third species from the Gulf of California is not formally described because the specimens are in poor condition. The new genus is characterized by having: 1) two distinctive body regions, the anterior with reduced parapodia lacking chaetae, and the posterior with long parapodia and chaetae and 2) a pair of large, elongate lensed eyes. These eyes are here described using histology and 3D reconstruction based on a Californian specimen. The two new species mainly differ in colour pattern, shape of parapodia, number of chaetae and body ciliation.