Some parasites are expected to have beneficial impacts on wild populations in polluted environments because of their bioaccumulation potential of pollutants from their hosts. The fate of organic micropollutants in host-parasite systems and the combined effect of parasitism and pollution were investigated in chub Squalius cephalus, a freshwater fish, infected (n = 73) or uninfected (n = 45) by acanthocephalan parasites Pomphorhynchus sp. from differently contaminated riverine sites. Several ubiquitous pollutants (polychlorinated biphenyls (PCBs), organochlorine pesticides (OCPs), polybrominated diphenyl-ethers (PBDEs), polycyclic aromatic hydrocarbons (PAHs), phthalates, insecticides, pyrethroids, and N,N-diethyl-meta-toluamide (DEET)) and some of their metabolites were characterized for the first time in parasites and various fish matrices (muscle, liver, and stomach content). Most organic pollutants reached higher levels in parasites than in chub matrices. In contrast, metabolite levels were lower in parasite tissues compared to fish matrices. Infected and uninfected chub exhibited no significant differences in their pollutant load. Body condition, organo-somatic indices, and immunity were not affected by parasitism, and few correlations were found with chemical pollution. Interestingly, infected chub exhibited lower oxidative damage compared to uninfected fish, irrespective of their pollutant load. In light of these results, this correlative study supports the hypothesis that acanthocephalan parasites could bring benefits to their hosts to cope with organic pollution.