The acquisition of nutrients is fundamental for the maintenance of bodily functions, growth, and reproduction in animals. As a result, fitness can be maximized only when animals are able to direct their attention to foods that reflect their current nutritional needs. Despite significant literature documenting the fitness consequences of nutrient composition and preference, less is known about the underlying genetic architecture of the dietary preferences themselves, specifically, the degree to which they can respond to selection. We addressed this by integrating evolutionary quantitative genetics and nutritional geometry to examine the shape of the sex-specific fitness surfaces and the availability of genetic variance for macronutrient preferences in the fruit fly Drosophila melanogaster. Combining these analyses, we found that the microevolutionary potential of carbohydrate and protein preference was above average in this population, because the expected direction of selection was relatively well aligned with the major axis of the genetic variance-covariance matrix, G. We also found that potential exists for sexually antagonistic genetic constraint in this system; macronutrient blends maximizing fitness differed between the sexes, and cross-sex genetic correlations for their consumption were positive. However, both sexes were displaced from their feeding optima, generating similar directional selection on males and females, with the combined effect being that minimal sex-specific genetic constraints currently affect dietary preferences in this population.