Flight is one of the most effective yet energetically demanding means of movement. Its energy costs are normally associated with interspecific variation in efficiency, size of organs, and physiological systems that reflect different flight capacities. Adaptive morphological variation may be constrained by physical demands that vary with body size, but work remains to place allometry associated with flight mode in an ecological and evolutionary context. We predicted that heart, lung, and skeletal masses, as well as tracheal diameter, should show a reciprocal positive correlation and have reduced size in species with poor flight capacities. We measured tracheal diameter together with lung, heart, and skeletal mass in 21 species of medium to large body sized game birds. We then compared 7 of these species categorized as short flyers belonging to the order Galliformes with 14 other species capable of sustained flapping flight. Our comparative analyses incorporating phylogeny revealed that once accounting for body mass, Galliformes had smaller heart mass compared to other species, as shown in few previous studies. Additionally, we detected reduced tracheal diameter and lung mass in Galliformes, suggesting the presence of morphological pleiotropy predicted under the concept of symmorphosis. These organs all showed different levels of reciprocal correlations due to their functional connection. Residual skeletal mass was independent of flight capacity and showed no relationship with heart mass, thus indicating that selection for reduced skeletal mass may have already maximized how light a bird skeleton can be, constraining mass-independent variation in this trait. Our results suggest that cardiorespiratory organs have evolved symmorphic variation in size that reflects costs and benefits associated with different flight capacities. However, our observed differences are confounded with phylogenetic history, so additional comparative studies are needed to rigorously test this hypothesis.