Abstract Parasitism is an important driver of ecosystem processes. Copepods are fundamental trophic links in marine food webs and harbour many microeukaryotic parasites, but unreliable access to infected individuals limits quantitative studies of parasite infection costs. Calanus spp., (helgolandicus or finmarchicus), infected with the Yellow-Hyphal Parasite become pigmented and are found near the surface, suggesting predator-mediated dispersal. Conventional markers prevented phylogenetic inference but confirmed that the parasite is not Ichthyophonus hoferi, as previously thought. We identified the pigments, quantified the pigment content and respiration rate, and derived stable isotope signatures of infected and uninfected Calanus spp. to examine costs of infection. We found that the pigments were astaxanthin and β-carotene, associated with the host and parasite, respectively. Parasitized hosts had increased astaxanthin content, reduced respiration rate, and lower lipid content. Ultrastructure imaging revealed parasitic cells associated with lipids in the haemocoel. The changes to host phenotype have detrimental impacts on energetics and the ecology of Calanus. We discuss the role of pigments in parasite-host interactions and suggest that the parasite produces β-carotene pigment for its physiological benefits. The trade-off between physiological benefits of pigments and conspicuousness for parasites is relevant in zooplankton-host systems, as zooplankton rely heavily on transparency for survival.