Identifying natural groups within the caenogastropod family Vermetidae has proven challenging. The sessile lifestyle of vermetids, with associated xenomorphically distorted, overgrown and corroded shells, has resulted in a long and confused taxonomic history based primarily on adult shell characters. In this study, we use morphological, anatomical and molecular data to clarify systematics and phylogenetic relationships within the genus Dendropoma s.l. We assess generic names previously used in the Dendropoma group for availability and recognize Veristoa Iredale, 1937, as a junior synonym of Dendropoma Mörch, 1861. We describe 21 species, eight of which are new, place them into four robustly supported genera (Dendropoma s.s.; Novastoa Finlay, 1926; Ceraesignum n. gen.; Cupolaconcha n. gen.), and outline the current state of knowledge of the distribution of these taxa. The genus Dendropoma s.s. is well supported in our phylogenetic analysis and is additionally supported by features of the operculum, reproductive traits and a novel mitochondrial gene order. Among the four genera, members of Dendropoma s.s. alone maintain unstalked egg capsules in the mantle cavity rather than attaching them to the shell via a slit in the female mantle. The opercula of examined species within the genus Novastoa are characterized by a well-developed mammilla on the internal surface and upright tightly packed spiral lamina on the external surface. In Ceraesignum n. gen., the operculum lacks a mammilla and displays a fingerprint-like texture on its inner surface. The genera Ceraesignum n. gen. and Novastoa form a well-supported monophyletic group with the genus Dendropoma s.s., although sister group relationships among these genera are not resolved. The fourth genus, Cupolaconcha n. gen. is more closely related to the vermetid genera Eualetes Keen, 1971a, Thylaeodus Mörch, 1860, and Petaloconchus Lea, 1843, demonstrating that Dendropoma s.l. is not a monophyletic group. The calcified operculum of Cupolaconcha n. gen. is unique in the Vermetidae and examined species in this genus are also characterized by a translocation of the valine mitochondrial tRNA. Further study will encompass the full range of morphological diversity in the Vermetidae to clarify the major lineages within this remarkable family of snails.