Abstract. The extraordinary parasitic metanauplius larva of Caribeopsyllus amphiodiae is sexually dimorphic, with conspicuous gonads, and elaborate lens‐bearing eyes. The parasites usually occur singly within their host, and grow for ≤5 months within the stomach of burrowing ophiuroids (Amphiodia urtica). They transform into free‐living, semelparous, non‐feeding adults that live only 2 weeks. The species' life‐history pattern, with a larval period ∼10 × longer than the adult life span, is contrariwise to that of other copepods but not for animals with non‐feeding adults of both sexes. It appears that the life cycle of C. amphiodiae is pedomorphic, and probably evolved through a delay of metamorphosis regulated by developmental hormones. We attribute the dominance of the larval phase to the greater potential for survival and growth of the enterozoic parasitic stages than of the free‐living, post‐metamorphic stages. We note that among marine invertebrates, non‐feeding adults of both sexes occur exclusively in taxa with a complex life cycle, and that non‐feeding adults of both sexes are never found in taxa that have small larvae and delayed maturation. They occur only when there is a large larva that can provide the adult stage with sufficient nutrient reserves for reproduction.