Vermicularia Lamarck, 1799 is a clade of Miocene–Recent gastropods with an unusual uncoiled shell morphology. Like other “worm-snails,” they are taxonomically troublesome, and although earlier work affirmed the turritellid affinity of one species, their systematic relationships have not otherwise been previously examined. Here, we present a molecular phylogeny of turritellids, including members of other previously named genera [Mesalia Gray, 1847; Zaria Gray, 1847; Torcula Gray, 1847; Protomella Thiele, 1929; Maoricolpus Finlay, 1926; and the recently named Turritellinella Harzhauser & Landau, 2019, represented by Turritellinella tricarinata (Brocchi, 1814) = “Turritella communis” Risso, 1826], to establish the monophyly of Vermicularia and determine higher level relationships. We provide a revised taxonomy with detailed diagnoses for all known living and fossil species of Vermicularia, including the synonymy of Vermicularia lumbricalis (Linnaeus, 1758) and the commonly used junior synonym Vermicularia knorrii (Deshayes, 1843). The new Miocene–Pliocene species Vermicularia katiae n. sp. is described from the Dominican Republic. The phylogenetic relationships within living and fossil Vermicularia are also established based on morphological characters and with close outgroup turritelliform species chosen based on the molecular phylogeny. Callostracum gracile (Maltzan, 1883) was found to be well nested among the other species and is reassigned to Vermicularia herein as Vermicularia gracilis (Maltzan, 1883). The reconstructed phylogeny indicates that new species arose via cladogenesis much more frequently than by anagenesis, with most lineages originating in the Pliocene, but prior to the complete closure of the Central American Seaway ∼ 3.5 million years ago.