The marine neogastropod family Costellariidae constitutes a large radiation encompassing 647 living species, widely distributed in tropical seas, with their highest diversity in the Central Indo-Pacific. The systematics of the family has undergone profound changes in the mid-2010s, when relationships within Costellariidae were critically revised based on molecular (multilocus) data from 80 species. Whereas four new genera were described, and two more transferred to Costellariidae from Ptychatractidae, relationships of some key lineages could not be resolved due to the incomplete taxonomic and geographic coverage. In the present study we combine an analysis of an extensive DNA-barcoding dataset with phylogenomics to propose a robust new phylogenetic hypothesis and revise the genus-level systematics of the family. Species delimitation was performed for a Cox1 dataset of 1475 specimens, which revealed 221 secondary species hypotheses (SSHs). The phylogeny was reconstructed from a 1003 loci dataset for 70 species representing all but two of the revealed major costellariid lineages. Maximum likelihood (ML) and Bayesian inference (BI) arrived at nearly identical topologies with full support for all backbone nodes but one, providing a robust framework for a new classification. We treat Turricostellaria as a synonym of Tosapusia. Further, based on a re-evaluation of the identity of the type species of Pusia, we conclude that the name should be applied to a Caribbean lineage, previously treated as a part of Vexillum. Consequently, the Indo-Pacific species of Pusia (Pusia) are here reassigned to a new genus Eupusia, and two other subgenera, Ebenomitra and Vexillena, are raised to full genera. Eight further new genera are described based on phylogenomics: Bathythala, Canaripusia and Caribbonus from the Caribbean in deep water, Pilgrivexillum, Pacifilux, Ponderiola and Cernohorskyola from the Central and southern Indo-Pacific, and Kilburniola from the south- western Indian Ocean. From a total of 25 SSHs corresponding to undescribed species, 23 are described herein in the genera Austromitra (1), Bathythala (1), Canaripusia (1), Caribbonus (3), Costapex (4), Eupusia (1), Kilburniola (1), Pilgrivexillum (1), Pusia (2), Thala (1), Tosapusia (1) and Vexillum (6).