In this study, we delved into the interaction between corallivorous marine gastropods, the muricid Coralliophilinae Chenu, 1859, and their cnidarian food targets. Coralliophilinae is a subfamily of specialised corallivorous caenogastropods that feed by browsing on octocorals or hexacorals. Only sparse information is available on the phylogenetic relationships and the degree of specificity of the trophic relationships within this corallivorous lineage. To address these gaps, we generated the largest molecular dataset to date, comprising two mitochondrial (cox1 and 16S rDNA) and one nuclear gene (ITS2 rDNA) from 586 specimens collected worldwide. The coral hosts of coralliophilines were identified through an integrative approach, combining literature data with new records, employing morphological and/or molecular markers, and incorporating data from DNA barcoding of the snail stomach content. Our comprehensive approach unveiled the existence of numerous cryptic species in Coralliophilinae, while the phylogeny showed that most of the currently accepted genera are not monophyletic. The molecular dating confirmed the origin of the Coralliophilinae in Middle Eocene, with diversification of most lineages during the Miocene. Our results indicate that the subfamily’s ancestor evolved in shallow waters in association with Scleractinia. Through the evolutionary history of Coralliophilinae, multiple host shifts to other cnidarian orders were observed, not correlated with changes in the depth range. The results of diversification analyses within the subfamily further suggest that the association with the host has influenced the evolutionary patterns of Coralliophilinae, but not vice versa.