We revise monotypic LeuceruthrusMarshall and Gilbert, 1905 (Azygiidae Lühe, 1909) by emending its generic diagnosis, redescribing its type species (Leuceruthrus micropteriMarshall and Gilbert, 1905), reassigning 2 species (Leuceruthrus stephanocauda [Faust, 1921] n. comb., Leuceruthrus ocalana [Smith, 1935] n. comb.), describing 2 new congeners (Leuceruthrus ksepkai n. sp. and Leuceruthrus blaisei n. sp.), and providing a phylogenetic analysis based on the internal transcribed spacer 2 (ITS2). Leuceruthrus is unique by having oblique preovarian testes, a vitellarium that does not extend anteriad into the forebody, and a uterus that is intercecal and between the ovary and ventral sucker. We describe the cercaria of Leuceruthrus cf. stephanocauda from cercariae shed from Elimia cf. carinifera and Elimia cf. modesta from Big Canoe Creek, Alabama. Leuceruthrus ksepkai n. sp. is described from cercariae shed from rasp elimia, Elimia floridensis (Reeve, 1860) from Holmes Creek, Florida, and Elimia sp. 1 from the Chocktawhatchee River, Florida. It differs from its congeners by the combination of having broadly rounded furcae with slight marginal pigmentation in live cercariae, no spines on the tail stem, distinct anterior and posterior ridges that flank the tail stem portion accommodating the withdrawn distome, minute protuberances occupying the lateral margin of the tail stem for its entire length, and protuberances that encircle the anterior third of the posterior tail stem (immediately posterior to the tail stem portion containing the withdrawn distome). Leuceruthrus blaisei n. sp. infects Elimia sp. and is the only known congener having proportionally small furcae (>tail stem maximum width) with a nipple-like distal projection and numerous minute projections on the tail stem surface. Our phylogenetic analysis included all of our new sequences plus all publicly available ITS2 sequences for Leuceruthrus spp. and Proteromera spp., and supported the monophyly of Leuceruthrus. It recovered L. ksepkai and L. cf. ksepkai in a polytomy, and Leuceruthrus blaisei as monophyletic (identical sequences), with L. micropteri and L. cf. stephanocauda recovered as sister taxa. The present study comprises the first systematic treatment of Leuceruthrus in over a century, the first description of a new species of Leuceruthrus in 117 yr, and the first taxonomic characterization of a species of Leuceruthrus from the Mobile River Basin. It also increases the number of accepted congeners from 1 to 5 and provides new host records (E. cf. carinifera and E. floridensis) for Leuceruthrus spp.