Humans and birds use very different running styles. Unlike humans, birds adopt “grounded running” at intermediate speeds—a running gait where at least one foot always maintains ground contact. Avian grounded running is a paradox: Animals usually minimize locomotor energy expenditure, but birds prefer grounded running despite incurring higher energy costs. Using predictive gait simulations of the emu (Dromaius novaehollandiae), we resolve this paradox by demonstrating that grounded running represents an optimal gait for birds, from both energetics and muscle excitations perspectives. Our virtual experiments decoupled effects of posture and tendon elasticity, biomechanically relevant anatomical features that cannot be isolated in real birds. The avian body plan prevents (near) vertical leg postures, making the running style used by humans impossible. Under this anatomical constraint, grounded running is optimal if the muscles produce the highest forces in crouched postures, as is true in most birds. Shared anatomical features suggest that, as a behavior, avian grounded running first evolved within non-avian dinosaurs.