Adaptive changes in organ size and physiology occur in most adult animals, but how these changes are regulated is not well understood. Previous research found that mating in females drives not only increases in gut size and stem cell proliferation but also alters feeding behavior, intestinal gene expression, and whole-body lipid storage, suggesting altered gut metabolism. Here, we show that mating dramatically alters female gut metabolism and digestive function. In addition to promoting a preference for a high-protein diet, mating also altered levels of TCA cycle intermediates and fatty acids in the gut, increased total gut lipids and protein, reduced relative carbohydrate levels, and enhanced the efficiency of protein digestion relative to carbohydrate digestion. The expression of genes that mediate each of these metabolic processes was similarly altered. In addition, we noted the mating-dependent downregulation of oxidative stress response and autophagy genes. Mating-dependent increases in ecdysone signaling played an important role in re-programming many, but not all, of these changes in the female gut. This study contributes to our understanding of how steroid signaling alters gut physiology to adapt to the demands of reproduction.