During human standing, tonic ankle extensor torque is required to support the centre of mass (CoM) forward of the ankles, and dynamic torque modulation is required to maintain unstable balance. Passive mechanisms contribute to both but the extent is controversial. Some groups have revealed a substantial intrinsic stiffness (65–90%) normalized to load stiffness, ‘mgh’. Others regard their methodology as unsuitable for the low-frequency conditions of quiet standing and believe the passive contribution to be small (10–15%). Here we applied low-frequency ankle rotations to upright subjects who were supported at the waist allowing the leg muscles to be passive and we report normalized stiffness. The passive calf muscles provided: (i) an extensor torque capable of sustaining unstable balance without tonic activity at a mean CoM–ankle angle of 1.6 deg, (ii) a long range stiffness of 13 ± 2% and (iii) a short range (< 0.2 deg) stiffness of 67 ± 8%. Chordal ankle stiffness, derived from the torque versus angle relationship for 7 deg rotations, shows a non-linear decrease (stiffness α rotation−0.33±0.04) from 101 ± 9% to 19 ± 5% for rotations of 0.03–7 deg, respectively. Thus, passive stiffness is well adapted for the continuum of postural and movement activity and has a substantial postural role eliminating the need for continuous muscle activity and increasing the unstable time constant of the human inverted pendulum. Ignoring the non-linear dependence of passive stiffness on sway size could lead to serious misinterpretation of experiments using perturbations and sensory manipulations such as eye closure, sway referencing and altered support surfaces.