Zanclea divergens is a tropical hydrozoan living in symbiotic association with bryozoans and currently reported from Papua New Guinea, Indonesia, and Maldives. Here, we used an integrative approach to assess the morpho-molecular diversity of the species across the Indo-Pacific. Phylogenetic and species delimitation analyses based on seven mitochondrial and nuclear loci revealed four well-supported molecular lineages corresponding to cryptic species, and representing a Pacific clade, an Indian clade, and two Red Sea clades. Since the general polyp morphology was almost identical in all samples, the nematocyst capsules were measured and analysed to search for possible fine-scale differences, and their statistical treatment revealed a significant difference in terms of length and width among the clades investigated. All Zanclea divergens specimens were specifically associated with cheilostome bryozoans belonging to the genus Celleporaria. The Pacific and Indian clades were associated with Celleporaria sp. and C. vermiformis, respectively, whereas both Red Sea lineages were associated with C. pigmentaria. Nevertheless, the sequencing of host bryozoans revealed that one of the Red Sea hydrozoan clades is associated with two morphologically undistinguishable, but genetically divergent, bryozoan species. Overall, our results show that Z. divergens is a species complex composed of morphologically cryptic lineages showing partially disjunct distributions and host specificity. The presence of two sympatric lineages living on the same host species reveal complex dynamics of diversification, and future research aimed at understanding their diversification process will likely improve our knowledge on the mechanisms of speciation among currently sympatric cryptic species.