Pollinator decline is strongly influenced by the spread of pathogens across species, yet most research has focused on honey bees and a narrow range of managed or wild pollinators. Cuckoo wasps (Hymenoptera: Chrysididae), a diverse family of cleptoparasitic and parasitoid insects, remain unstudied in this context despite their dual role as floral visitors and nest parasites of solitary bees and wasps. This study investigated whether cuckoo wasps could host bee-associated pathogens, including viruses, microsporidia and trypanosomatids. Specimens were collected at two Italian sites with contrasting environmental conditions and analysed individually using quantitative PCR. In total, 343 hymenopterans were screened, including 84 cuckoo wasps representing 21 species. All pathogens except Crithidia mellificae were detected. Pathogen prevalence and abundance varied significantly between sites, with higher values of deformed wing virus (DWV) and C. bombi at the montane site, and greater prevalence of Nosema ceranae and acute bee paralysis virus (ABPV) at the lowland site, indicating strong environmental influences. Cuckoo wasps generally showed lower DWV prevalence than wild bees but higher prevalence of C. bombi and black queen cell virus (BQCV). Strikingly, host–parasite pairs such as Chrysis rufitarsis and Hoplitis laevifrons shared nearly the full pathogen set, suggesting direct transmission through parasitic interactions in addition to environmental and floral pathways. The obtained findings provide the first evidence that cuckoo wasps host a broad range of pollinator pathogens. By linking floral and nest-based transmission routes, cuckoo wasps may play a pivotal ecological role within pathogen networks. These results highlighted the need to include parasitic taxa in pathogen surveillance to better understand pollinator health and ecosystem resilience.