Animals adjust resource acquisition throughout life to meet changing physiological demands of growth, reproduction, activity and somatic maintenance. Wing-polymorphic crickets invest in either dispersal or reproduction during early adulthood, providing a system in which to determine how variation in physiological demands, determined by sex and life history strategy, impact nutritional targets, plus the consequences of nutritionally imbalanced diets across life stages. We hypothesized that high demands of biosynthesis (especially oogenesis in females) drive elevated resource acquisition requirements and confer vulnerability to imbalanced diets. Nutrient targets and allocation into key tissues associated with life history investments were determined for juvenile and adult male and female field crickets (Gryllus lineaticeps) when given a choice between two calorically equivalent but nutritionally imbalanced (protein- or carbohydrate-biased) artificial diets, or when restricted to one imbalanced diet. Flight muscle synthesis drove elevated general caloric requirements for juveniles investing in dispersal, but flight muscle quality was robust to imbalanced diets. Testes synthesis was not costly, and life history investments by males were insensitive to diet composition. In contrast, costs of ovarian synthesis drove elevated caloric and protein requirements for adult females. When constrained to a carbohydrate-biased diet, ovary synthesis was reduced in reproductive morph females, eliminating their advantage in early life fecundity over the dispersal morph. Our findings demonstrate that nutrient acquisition modulates dispersal–reproduction trade-offs in an age- and sex-specific manner. Declines in food quality will thus disproportionately affect specific cohorts, potentially driving demographic shifts and altering patterns of life history evolution.