The evolution of bipedal gait is a key adaptive feature in hominids, but the running abilities of early hominins have not been extensively studied. Here, we present physics simulations of Australopithecus afarensis that demonstrate this genus was mechanically capable of bipedal running but with absolute and relative (size-normalized) maximum speeds considerably inferior to modern humans. Simulations predicted running energetics for Australopithecus that are generally consistent with values for mammals and birds of similar body size, therefore suggesting relatively low cost of transport across a limited speed range. Through model parameterization, we demonstrate the key role of ankle extensor muscle architecture (e.g., the Achilles tendon) in the evolution of hominin running energetics and indeed in an increase in speed range, which may have been intrinsically coupled with enhanced endurance running capacity. We show that skeletal strength was unlikely to have been a limiting factor in the evolution of enhanced running ability, which instead resulted from changes to muscle anatomy and particularly overall body proportions. These findings support the hypothesis that key features in the human body plan evolved specifically for improved running performance and not merely as a byproduct of selection for enhanced walking capabilities.