Fear of predation can disappear rapidly in the absence of predators, as bolder individuals outcompete vigilant individuals for food and mates. To examine the evolution of fear in a seasonal environment, we exposed Drosophila melanogaster to mantid predators during the breeding season and the non-breeding season, and compared these with a control. We compared three Drosophila lineages that were maintained in captivity for (1) ∼45 years without mantid predators, (2) ∼5 years without mantid predators, and (3) ∼5 years with mantid predators (predator-evolved). The presence of a predator during the non-breeding season caused reduced fecundity in the following breeding season, independent of the evolutionary lineage. However, the presence of a predator during reproduction caused offspring to emerge earlier, and this effect was more pronounced in the predator-evolved lineage. Thus, the fear response was related to evolutionary lineage only during the larval life stage, which is when foraging competition, and hence the cost of fear, may be highest. We present one of the first experimental demonstrations that emotion (fear) can evolve in response to environmental context.