Many trophically transmitted parasites have complex life cycles: they pass through at least one intermediate host before reproducing in their final host. Despite their economic and theoretical importance, the evolution of such cycles has rarely been investigated. Here, combining a novel modeling approach with experimental data, we show for the first time that an optimal transfer time between hosts exists for a “model parasite,” the tapeworm Schistocephalus solidus, from its first (copepod) to its second (fish) intermediate host. When transferring between hosts around this time, (1) parasite performance in the second intermediate host, (2) reproductive success in the final host, and (3) fitness in the next generation is maximized. At that time, the infected copepod's behavior changes from predation suppression to predation enhancement. The optimal time for switching manipulation results from a trade-off between increasing establishment probability in the next host and reducing mortality in the present host. Our results show that these manipulated behavioral changes are adaptive for S. solidus, rather than an artifact, as they maximize parasite fitness.