To clarify the systematic positions of the important gonyaulacacean genera Operculodinium Wall, 1967 emend. Matsuoka et al., 1997 and Protoceratium Bergh, 1881, we present in detail the tabulation of the Oligocene–Pleistocene, thermophilic, cyst-defined species Operculodinium bahamense Head in Head and Westphal, 1999 emend., and the extant, cosmopolitan, theca-defined species Protoceratium reticulatum (Claparède and Lachmann, 1859) Bütschli, 1885. Both species have a sexiform hyposomal tabulation, and L-type (Protoceratium reticulatum) or modified L-type (Operculodinium bahamense) ventral organization. Protoceratium reticulatum has dextral torsion of the hypotheca, requiring assignation of the genus to the subfamily Cribroperidinioideae Fensome et al., 1993, whereas Operculodinium bahamense has neutral torsion requiring assignation to the subfamily Leptodinioideae Fensome et al., 1993. The stratigraphic range of this subfamily is now extended upwards to the lower Pleistocene. Paradoxically, Protoceratium reticulatum produces a cyst whose morphology is circumscribed by the cyst-defined genus Operculodinium, either implying polyphyletic origins for this genus or that combinations of ventral organization and torsion used to subdivide the family Gonyaulacaceae cannot always be applied rigidly. In detail, Operculodinium bahamense is shown to have an unusual ventral tabulation in which the first apical plate contacts the apical pore complex but not the sulcus. The new term “episert” is proposed to describe this plate relationship, which appears to have evolved independently in several lineages of the suborder Gonyaulacineae.