As a fundamental ecological aspect of most organisms, locomotor function significantly constrains morphology. At the same time, the evolution of novel locomotor abilities has produced dramatic morphological transformations, initiating some of the most significant diversifications in life history. Despite significant new fossil evidence, it remains unclear whether volant locomotion had a single or multiple origins in pennaraptoran dinosaurs and the volant abilities of individual taxa are controversial. The evolution of powered flight in modern birds involved exaptation of feathered surfaces extending off the limbs and tail yet most studies concerning flight potential in pennaraptorans do not account for the structure and morphology of the wing feathers themselves. Analysis of the number and shape of remex and rectrix feathers across a large dataset of extant birds indicates that the number of remiges and rectrices and the degree of primary vane asymmetry strongly correlate with locomotor ability revealing important functional constraints. Among these traits, phenotypic flexibility varies reflected by the different rates at which morphological changes evolve, such that some traits reflect the ancestral condition, whereas others reflect current locomotor function. While Mesozoic birds and Microraptor have remex morphologies consistent with extant volant birds, that of anchiornithines deviate significantly providing strong evidence this clade was not volant. The results of these analyses support a single origin of dinosaurian flight and indicate the early stages of feathered wing evolution are not sampled by the currently available fossil record.