Parasites are ubiquitous in natural systems and ecosystem-level effects should be proportional to the amount of biomass or energy flow altered by the parasites. Here we quantified the extent to which a manipulative parasite altered the flow of energy through a forest-stream ecosystem. In a Japanese headwater stream, camel crickets and grasshoppers (Orthoptera) were 20 times more likely to enter a stream if infected by a nematomorph parasite (Gordionus spp.), corroborating evidence that nematomorphs manipulate their hosts to seek water where the parasites emerge as free-living adults. Endangered Japanese trout (Salvelinus leucomaenis japonicus) readily ate these infected orthopterans, which due to their abundance, accounted for 60% of the annual energy intake of the trout population. Trout grew fastest in the fall, when nematomorphs were driving energy-rich orthopterans into the stream. When infected orthopterans were available, trout did not eat benthic invertebrates in proportion to their abundance, leading to the potential for cascading, indirect effects through the forest-stream ecosystem. These results provide the first quantitative evidence that a manipulative parasite can dramatically alter the flow of energy through and across ecosystems.