Learning is thought to be adaptive in variable environments, whereas constant, predictable environments are supposed to favor unconditional, genetically fixed responses. A dichotomous view of behavior as either learned or innate ignores a potential evolutionary interaction between the learned and innate components of a behavioral response. We addressed this interaction in the context of oviposition substrate choice in Drosophila melanogaster, asking two main questions. First, will learning also evolve in a constant environment in which it always pays to show the same choice? Second, how does an opportunity to learn affect the evolution of the innate (genetic) component of oviposition substrate choice? We exposed experimental populations to four selection regimes, involving selection on oviposition substrate preference (an orange versus a pineapple medium). In two selection regimes the flies were selected for preference either for the orange medium, or for the pineapple medium. In the remaining two selection regimes the flies were also selected for preference for either orange or pineapple, but additionally could use past experience (aversion learning) to decide which medium it paid to avoid. Lines exposed to the latter selection regimes evolved improved learning ability, indicating that learning may be advantageous even if the same behavioral response is favored every generation. Furthermore, of the two selection regimes that favored oviposition on the pineapple medium, the regime that allowed for learning led to the evolution of a stronger innate preference for pineapple, than the regime that did not allow for learning. In contrast, of the two regimes that selected for oviposition on the orange medium, the one that allowed for learning led to a smaller evolutionary change of the innate preference. Thus, an opportunity to learn facilitated the evolution of innate preference under selection for preference for pineapple, but hindered it under selection for preference for orange. We discuss possible mechanisms for this effect.