It has been unclear whether the perception of depth from motion parallax is an entirely visual process or whether it requires extra-retinal information such as head movements, vestibular activation, or eye movements. Using a motion aftereffect and static test stimulus technique to eliminate visual cues to depth, this psychophysical study demonstrates that the visual system employs a slow eye movement signal, optokinetic response (OKR) in particular, for the unambiguous perception of depth from motion parallax. A vestibular signal, or vestibularly driven eye movement signal is insufficient for unambiguous depth from motion parallax. Removal of the OKR eye movement signal gives rise to ambiguous perceived depth in motion parallax conditions. Neurophysiological studies suggest a possible neural mechanism in medial temporal and medial superior temporal cortical neurons that are selective to depth, motion, and direction of eye movement.