The Splanchnotrophidae is a family of highly modified endoparasitic copepods known to infest nudibranch or sacoglossan sea slug hosts. Most splanchnotrophid species appear to be specific to a single host, but some were reported from up to nine different host species. However, splanchnotrophid taxonomy thus far is based on external morphology, and taxonomic descriptions are, mostly, old and lack detail. They are usually based on few specimens, with intraspecific variability rarely reported. The present study used molecular data for the first time to test (1) the current taxonomic hypotheses, (2) the apparently strict host specificity of the genus Ismaila and (3) the low host specificity of the genus Splanchnotrophus with regard to the potential presence of cryptic species. Phylogenetic analyses herein used sequences of the barcoding region of the cytochrome oxidase I (COI) gene from 40 specimens representing 13 species of five genera. Species delimitation approaches include distance and barcoding gap analyses, haplotype networks and diagnostic nucleotides. Molecular results are largely compatible with the commonly accepted, morphology-based taxonomy of the Splanchnotrophidae. Strict host specificity could be confirmed for two Ismaila species. COI analyses also supported the idea that Splanchnotrophus angulatus is host-promiscuous. In Ismaila, morphology seems more suitable than barcoding to display speciation events via host switches in a recent Chilean radiation. In Splanchnotrophus, some genetic structure suggests ongoing diversification, which should be investigated further given the inadequate morphology-based taxonomy. The present study thus supports the presence of two different life history strategies in splanchnotrophids, which should be explored integratively.