Allopodocotyle enkaimushi n. sp. (Opecoelidae: Plagioporinae) is described from the pyloric ceca and intestine of the short-tail grenadier, Nezumia proxima (Smith and Radcliff, 1912) (Gadiformes, Macrouridae), collected at depths of 681–1,061 m off Jōgashima Island, Sagami Bay, Japan. The new species is placed in Group C and is distinguished from its closest congener, Allopodocotyle margolisi Gibson, 1995, by possessing a terminal rather than a subterminal oral sucker; an unspecialized, inconspicuously elevated ventral sucker rather than being embedded in a well-developed ventral eminence that forms an anterior and lateral fold but with no distinct, muscular fold around the entire ventral sucker; a cirrus pouch that is entirely anterior to the ventral sucker rather than extending posteriorly to about the midlevel of it; and a sessile genital pore that is not situated on an eminence and surrounded by a muscular thickening of the body wall that appears to form a sphincter, as is the case in A. margolisi. In addition, A. enkaimushi n. sp. parasitizes a member of the grenadier genus Nezumia Jordan, 1904, from the west Pacific Ocean (Japan) rather than a species of the grenadier genus Coryphaenoides Gunnerus, 1765, from the North Atlantic Ocean. The combination of tandem testes, an entirely pre-acetabular cirrus pouch, and a pre-bifurcal (esophageal level) genital pore distinguishes A. enkaimushi n. sp. from all members of Group C recognized herein as well as from the 3 accepted species of Allopodocotyle Pritchard, 1966, already known from Japanese waters. A checklist of parasites reported from N. proxima is provided. We also furnish a key to the species in Groups A–C of Allopodocotyle, offer insights into the host familial diversity of shallow-water representatives in this genus, and hypothesize life histories for the 2 deep-water representatives in this genus.