Failure to adapt to a changing nutritional environment comes at a cost, as evidenced by the modern human obesity crisis. Consumption of energy-rich diets can lead to obesity and is associated with deleterious consequences not only in humans but also in many other animals, including insects. The question thus arises whether animals restricted over multiple generations to high-energy diets can evolve mechanisms to limit the deposition of adverse levels of body fat. We show that Plutella xylostella caterpillars reared for multiple generations on carbohydrate-rich foods (either a chemically defined artificial diet or a high-starch Arabidopsis mutant) progressively developed the ability to eat excess carbohydrate without laying it down as fat, providing strong evidence that excess fat storage has a fitness cost. In contrast, caterpillars reared in carbohydrate-scarce environments (a chemically defined artificial diet or a low-starch Arabidopsis mutant) had a greater propensity to store ingested carbohydrate as fat. Additionally, insects reared on the low-starch Arabidopsis mutant evolved a preference for laying their eggs on this plant, whereas those selected on the high-starch Arabidopsis mutant showed no preference. Our results provide an experimental example of metabolic adaptation in the face of changes in the nutritional environment and suggest that changes in plant macronutrient profiles may promote host-associated population divergence.