The size of digestive organs can be rapidly and reversibly adjusted to ecological circumstances, but such phenotypic flexibility comes at a cost. Here, we test how the gizzard mass of a long-distance migrant, the red knot (Calidris canutus), is adjusted to (i) local climate, (ii) prey quality and (iii) migratory fuelling demands. For eight sites around the world (both wintering and stopover sites), we assembled data on gizzard masses of free-living red knots, the quality of their prey and the local climate. Using an energetic cost–benefit approach, we predicted the gizzard size required for fastest fuelling (net rate-maximization, i.e. expected during migration) and the gizzard size required to balance daily energy budgets (satisficing, expected in wintering birds) at each site. The measured gizzards matched the net rate-maximizing predictions at stopover sites and the satisficing predictions at wintering sites. To our surprise, owing to the fact that red knots selected stopover sites with prey of particularly high quality, gizzard sizes at stopovers and at wintering sites were nevertheless similar. To quantify the benefit of minimizing size changes in the gizzard, we constructed a model incorporating the size-dependent energy costs of maintaining and carrying a gizzard. The model showed that by selecting stopovers containing high-quality prey, metabolic rates are kept at a minimum, potentially reducing the spring migratory period by a full week. By inference, red knots appear to time their stopovers so that they hit local peaks in prey quality, which occur during the reproductive seasons of the intertidal benthic invertebrates.