The evolution of powered flight has traditionally been associated with the origin of birds, the most successful clade of modern tetrapods, as exemplified by the nearly 10,000 species alive today. Flight requires a suite of morphological changes to skeletal anatomy to create a light yet resistant framework for an airfoil and advanced nervous motor control. Given the level of morphological integration necessary to create a suitable aerofoil, the origin of flight may be intuitively assumed to be coupled with high evolutionary rates of wing-related morphologies. Here we show that the origin of birds is associated with little or no evolutionary change to the skeletal anatomy of the forelimb, and thus Archaeopteryx is unlikely to be the “Rosetta Stone” for the origin of flight it was once believed to be. Using comparative statistics and time-series analyses on a data set constructed from all known forelimb skeletal anatomy of non-avian theropod dinosaurs and a diverse assemblage of early birds, we demonstrate three focused peaks of rapid forelimb evolution at Tetanurae, Eumaniraptora, and Ornithothoraces. The peaks are not associated with missing data and remain stable under multiple perturbations to the phylogenetic arrangements. Different regions of the forelimbs are demonstrated to have undergone asynchronous periods of evolutionary peaks and stasis. Our results evince a more complicated stepwise mode of forelimb evolution before and after the origin of Aves than previously supposed.