We herein redescribe the enigmatic Cathariotrema selachii (MacCallum, 1916) Johnston and Tiegs, 1922 based on the holotype, paratypes, and newly collected specimens infecting the olfactory organ of 5 shark species from the Gulf of Mexico (all new host records): scalloped hammerhead shark, Sphyrna lewini (Griffith and Smith, 1834) (Carcharhiniformes: Sphyrnidae); great hammerhead shark, Sphyrna mokarran (Rüppell, 1837); blacktip shark, Carcharhinus limbatus (Müller and Henle, 1839) (Carcharhiniformes: Carcharhinidae); spinner shark, Carcharhinus brevipinna (Müller and Henle, 1839); and Atlantic sharpnose shark, Rhizoprionodon terraenovae (Richardson, 1836) (Carcharhinidae). These specimens were morphologically indistinguishable from each other and from MacCallum's holotype and paratypes. Those sequenced had identical first internal transcribed spacer (ITS1) and large subunit ribosomal DNA (28S) nucleotide sequences. As such, C. selachii infects sharks of 2 orders (Carcharhiniformes, Lamniformes) and 3 families (Carcharhinidae, Sphyrnidae, Lamnidae) in the Northwestern Atlantic Ocean (type locality) and Gulf of Mexico (new records herein). This report is the first of new specimens of C. selachii in the Atlantic Ocean Basin in 95 yr and corrects long-standing error cascades and ambiguities concerning the morphology and systematic placement of C. selachii. Considering morphology and nucleotide-based phylogenetic evidence (28S, Bayesian analysis), we herein emend monotypic CathariotremaJohnston and Tiegs, 1922 and propose Cathariotrematinae Bullard n. subfam. for it and 4 other genera (all formerly assigned to Merizocotylinae Johnston and Tiegs, 1922). These genera comprise species infecting only the nose of sharks (monotypic Cathariotrema, SqualotremaKearn and Green, 1983 and SeptitremaKheddam, Chisholm, and Tazerouti, 2020 plus 3 species of TriloculotremaKearn, 1993) and nose of a chimaera (monotypic HolocephalocotyleDerouiche, Neifar, Gey, Justine, and Tazerouti, 2019). Cathariotrematinae differs from Merizocotylinae by having a 3-part attachment organ and by lacking open loculi that symmetrically encircle a cluster of >2 loculi in the center of the haptor. Monophyletic Cathariotrematinae (with sequences representing species of Cathariotrema, Triloculotrema, and Holocephalocotyle only) was sister to monophyletic Merizocotylinae, which together were sister to monophyletic Calicotylinae Monticelli, 1903. These subfamilies comprise a monophyletic group of monocotylids that have a double vagina and infect extrabranchial, enclosed niches (urogenital system, body cavity, olfactory chamber/nose) on their shark, ray, and chimaera hosts (all other monocotylids have a single vagina and infect the gill or body surfaces of rays only). Monocotylinae Taschenberg, 1879 and Decacotylinae Chisholm, Wheeler, and Beverley-Burton, 1995 were recovered as monophyletic. Heterocotylinae Chisholm, Wheeler, and Beverley-Burton, 1995 remained paraphyletic. We accept ParacalicotyleSzidat, 1970.