Abstract Background Ecological constraints related to foraging are expected to affect the evolution of morphological traits relevant to food capture, manipulation and transport. Females of central-place foraging Hymenoptera vary in their food load manipulation ability. Bees and social wasps modulate the amount of food taken per foraging trip (in terms of e.g. number of pollen grains or parts of prey), while solitary wasps carry exclusively entire prey items. We hypothesized that the foraging constraints acting on females of the latter species, imposed by the upper limit to the load size they are able to transport in flight, should promote the evolution of a greater load-lifting capacity and manoeuvrability, specifically in terms of greater flight muscle to body mass ratio and lower wing loading. Results Our comparative study of 28 species confirms that, accounting for shared ancestry, female flight muscle ratio was significantly higher and wing loading lower in species taking entire prey compared to those that are able to modulate load size. Body mass had no effect on flight muscle ratio, though it strongly and negatively co-varied with wing loading. Across species, flight muscle ratio and wing loading were negatively correlated, suggesting coevolution of these traits. Conclusions Natural selection has led to the coevolution of resource load manipulation ability and morphological traits affecting flying ability with additional loads in females of central-place foraging Hymenoptera. Release from load-carrying constraints related to foraging, which took place with the evolution of food load manipulation ability, has selected against the maintenance of a powerful flight apparatus. This could be the case since investment in flight muscles may have to be traded against other life-history traits, such as reproductive investment.