Nutrition is an important determinant of an animal's survival and fitness. Phenotypic plasticity allows a genotype to adjust life history traits to changes in its nutritional environment, and it varies among individuals. The origin of this variation comes from differences in proximate mechanisms regulating trait expression. To understand how variation in plasticity is achieved, we made use of a Drosophila melanogaster isogenic panel to characterize nutritional plasticity for fecundity by feeding flies diets differing in their yeast content and counting the number of eggs produced. We then identified lines with the highest and lowest plastic responses to diet, and dissected the potential proximate mechanisms responsible for these differences in plasticity, including morphology, behaviour, and physiology. Our results suggest that variation in plasticity is not due to differences in ovariole number, but due to both increased food intake, and higher efficiency at converting food into eggs. Our results show that, in this population of D. melanogaster, variation in behaviour and physiology, but not morphology, underlies differences in plasticity for fecundity. Further, they set the stage for future studies aiming to understand how the proximate mechanisms that generate genetic variation in plasticity contribute to a population's persistence when faced with environmental changes.