Given a finite amount of resources, a central requirement of all organisms is optimizing the allocation of those resources to competing anatomical structures and physiological functions, which necessitates the coordination of multiple organ systems within the nutritional environment. The insulin/insulin-like growth factor signaling (IIS) pathway is known to influence the coordination of nutrition with metabolism and allocation of nutrients, but little is known about the genetic basis of standing variation in the pathway. Most studies to date of the IIS pathway have followed a "one gene at a time" approach. In this regard, they have been very successful at determining the pathway's role in the regulation of metabolism and resource allocation and of the effects of altering each gene in isolation. In stark contrast to this success, we know little about the genetic basis of natural variation in the IIS pathway, metabolism, and resource allocation. We utilize a large multiparental mapping population, the Drosophila Synthetic Population Resource to map QTL for transcript levels of the genes encoding the core components of the IIS pathway in three different nutritional environments. We identify the loci responsible for the response of IIS expression in different nutritional conditions and discuss the extent to which different loci control IIS expression in different environmental conditions.