Assessment of the energetic costs of parasitism is central to understanding the role of parasites in their hosts' foodwebs, but few studies have directly measured these costs. This study demonstrates that infection with the acanthocephalan parasite Acanthocephalus tehlequahensis causes a significant and direct energetic cost to its freshwater isopod intermediate host Ceacidotea communis at both individual and population levels. Bomb calorimetry was used to measure energy (kj·m−2.y−1) allocated to host growth, reproduction, and respiration in infected and uninfected isopods and to parasite tissue in infected isopods. Infected isopod individuals allocated ~21% of their net production energy to parasite growth, and they were larger (length), consumed more leaf detritus, and lost significantly more energy to respiration than uninfected controls (P ≤ 0.05). They also allocated proportionally less energy to tissue growth, allocated zero energy to reproduction, and were less efficient at converting energy into isopod biomass when compared to uninfected controls (P ≤ 0.05). In the field, isopod populations were surveyed monthly for a year. The parasite had a mean infection prevalence in the stream of 30.19% ± 8.31 SE with a mean intensity of 1.12 ± 0.39 SE parasites/host in the population, and based on this infection rate, it is estimated that ∼6.7% of total production energy of the isopod population (infected and uninfected) is diverted towards the parasite.