The ostrich (Struthio camelus) is the largest extant biped. Being flightless, it exhibits advanced cursorial abilities primarily evident in its characteristic speed and endurance. In addition to the active musculoskeletal complex, its powerful pelvic limbs incorporate passive structures wherein ligaments interact with joint surfaces, cartilage and other connective tissue in their course of motion. This arrangement may enable energy conservation by providing joint stabilisation, optimised limb segment orientation and automated positioning of ground contact elements independently of direct muscle control. The intertarsal joint is of particular interest considering its position near the mid-point of the extended limb and its exposure to high load during stance with significant inertial forces during swing phase. Functional-anatomical analysis of the dissected isolated joint describes the interaction of ligaments with intertarsal joint contours through the full motion cycle. Manual manipulation identified a passive engage-disengage mechanism (EDM) that establishes joint extension, provides bi-directional resistance prior to a transition point located at 115 degrees and contributes to rapid intertarsal flexion at toe off and full extension prior to touch down. This effect was subsequently quantified by measurement of intertarsal joint moments in prepared anatomical specimens in a neutral horizontal position and axially-loaded vertical position. Correlation with kinematic analyses of walking and running ostriches confirms the contribution of the EDM in vivo. We hypothesise that the passive EDM operates in tandem with a stringently coupled multi-jointed muscle-tendon system to conserve the metabolic cost of locomotion in the ostrich, suggesting that a complete understanding of terrestrial locomotion across extinct and extant taxa must include functional consideration of the ligamentous system.