Morphological scaling relationships between the sizes of individual traits and the body captures the characteristic shape of a species, and the evolution of scaling is the primary mechanism of morphological diversification. However, we have almost no knowledge of the genetic architecture of scaling, critical if we are to understand how scaling evolves. Here we explore the genetic architecture of population-level morphological scaling relationships – the scaling relationship fit to multiple genetically-distinct individuals in a population – by describing the distribution of individual scaling relationships – genotype-specific scaling relationships that are unseen or cryptic. These individual scaling relationships harbor the genetic variation that determines relative trait growth within individuals, and theory suggests that their distribution dictates how the population scaling relationship will respond to selection. Using variation in nutrition to generate size variation within 197 isogenic lineages of Drosophila melanogaster, we reveal extensive variation in the slopes of the wing-body and leg-body scaling relationships among individual genotypes. This genetic variation reflects variation in the nutritionally-induced size plasticity of the wing, leg and body. Surprisingly, we find that variation in the slope of individual scaling relationships primarily results from variation in nutritionally-induced plasticity of body size, not leg or wing size. These data allow us to predict how different selection regimes alter scaling in Drosophila and is the first step in identifying the genetic targets of such selection. Our approach provides a general framework for understanding the genetic architecture of scaling, an important prerequisite to explaining how selection changes scaling and morphology.