Gastropods of over a dozen genera in the family Eulimidae have been identified as parasites of brittle stars, and many more remain to be discovered and described for a comprehensive understanding of the evolutionary history of their host–parasite relationships. In this study, we describe Fusceulimoides kohtsukai gen. et sp. nov., parasitic on the little brittle star, Ophiactis savignyi (Ophiactidae), in Kanagawa, central Japan. The new genus is distinguished from other eulimid genera by the combination of following seven conchological characters: (1) a very small size of up to 1.7 mm high, (2) a colorless translucent appearance, (3) a conical pupiform shape with a paucispiral protoconch, (4) slightly convex teleoconch whorls, (5) a remarkably large body whorl occupying 65–70% of the total shell height, (6) a broad, somewhat squarish and laterally expanded aperture with a strongly curved outer lip, and (7) a developed parietal callus without an indentation or depression in the umbilical area. A multi-locus molecular phylogeny revealed its distant relationship to Hemiliostraca + Pyramidelloides, a previously known clade of ophiuroid parasites, thereby suggesting multiple origins of this host–parasite association in Eulimidae.