Ovipositing insects face at least four decisions: 1) what hosts to utilize, 2) where to search for them, 3) what clutch size, and 4) what sex ratio to produce on a host. Historically, study of these phenomena has focused on elucidating the proximate causes of observed behaviors. However, as originally outlined by N. Tinbergen, three other “causes” are also important in fully understanding any pattern of behavior. These are ontogenetic, phylogenetic, and ultimate (or natural selection) causes. Here we advocate study of all four types of causation, viewing them as complementary. We then discuss each of the oviposition decisions in light of natural selection theory to illustrate the utility of understanding the selective forces acting on ovipositing females.