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Bentholebouria colubrosa gen. n. et sp. n. (Digenea: Opecoelidae) is described in the wenchman, Pristipomoides aquilonaris, from the eastern Gulf of Mexico, and new combinations are proposed: Bentholebouria blatta comb. n., Bentholebouria longisaccula comb. n., Bentholebouria rooseveltiae comb. n., and Bentholebouria ulaula comb. n. The new genus is morphologically similar to Neolebouria, but with a longer cirrus sac, entire testes, a rounded posterior margin with a cleft, and an apparent restriction to the deepwater snappers. Morphologically, the new species is closest to B. blatta from Pristipomoides argyrogrammicus off New Caledonia but can be differentiated by the nature of the internal seminal vesicle (2-6 turns or loops rather than constrictions), a longer internal seminal vesicle (occupying about 65% rather than 50% of the cirrus sac), a cirrus sac that extends further into the hindbody (averaging 136% rather than 103% of the distance from the posterior margin of the ventral sucker to the ovary), and a narrower body (27% rather than 35% mean width as % of body length). A Bayesian inference analysis of partial sequence of the 28S rDNA from Neolebouria lanceolata, Cainocreadium lintoni, Hamacreadium mutabile, Opecoeloides fimbriatus, Podocotyloides brevis, the new species, and previously published comparable sequences from 10 opecoelid species revealed two clades. One clade includes deep-sea (more or equal 200 m) and freshwater fish opecoelids + Opecoeloides Bremser, and a second clade included those opecoelids from shallow-water marine, perciform fishes.