The family Cocculinidae (Gastropoda: Cocculinida) consists of small, usually colourless benthic limpets living primarily at depths below 100 m, and on decaying plant or animal remains. These habitats are difficult to sample and the knowledge about Cocculinidae species diversity, biogeography, ecology and evolution is therefore poor. To explore the species diversity of the Cocculinidae, we examined 499 specimens collected from 196 sites, mainly explored during expeditions of the ‘Tropical Deep-Sea Benthos’ programme in the Indo-West Pacific (IWP). To propose a species hypotheses, we used an integrated approach to taxonomy in which we combined DNA-based methods, with morphological, geographical and ecological considerations. To classify the species hypotheses into genera, we used a combination of one mitochondrial and two nuclear gene fragments to reconstruct a phylogenetic tree. We then used six morphological characters to diagnose the identified genera. Our results revealed an exceptionally high diversity of IWP Cocculinidae, with 51 species hypotheses that were mostly not assigned to available species names. We also discovered a previously unknown type of copulatory structure in the group. At a higher taxonomic level, we identified ten main clades in the family. Although six of them matched existing genera, four others should be regarded as new genera awaiting formal description.