A new genus and species of Nerillidae, Nipponerilla irabuensis gen. nov., sp. nov., is described from an anchialine cave in Shimoji Island, west of Irabu Island (Miyako Islands, Southwestern Japan). Its morphology was examined with light, scanning electron, and confocal laser scanning microscopy. This new species, along with two putative new cave species from the Turks and Caicos Islands and several closely related nerillids, was included in a phylogenetic analysis employing five concatenated gene markers (16S rRNA, 18S rRNA, 28S rRNA, H3, and COI). Nipponerilla irabuensis gen. nov., sp. nov. was found to be sister taxon to the cave-exclusive genus Speleonerilla Worsaae, Sterrer & Iliffe, in Worsaae et al., 2019, but shows morphological resemblance to both Speleonerilla and Mesonerilla Remane, 1949. Thus, Nipponerilla gen. nov. constitutes a new monotypic genus in Nerillidae diagnosed by a combination of the following characters: nine segments, compound chaetae, high palp and antennae to body length ratios, and gonochoristic reproduction with two pairs of spermioducts opening in segments VII and VIII. Its placement among Nerillidae is discussed, along with its putative adaptations to an anchialine environment.