Little is known about the three-dimensional characteristics of vestibulo-collic reflexes during natural locomotion. Here we determined how well head stability is maintained by the angular and linear vestibulo-collic reflexes (aVCR, lVCR) during quadruped locomotion in rhesus and cynomolgus monkeys. Animals walked on a treadmill at velocities of 0.4-1.25 m/s. Head rotations were represented by Euler angles (Fick convention). The head oscillated in yaw and roll at stride frequencies (1-2Hz) and pitched at step frequencies (2-4Hz). Head angular accelerations (100/°s²-2,500°/s²) were sufficient to have excited the aVOR to stabilize gaze. Pitch and roll head movements were less than 7°, peak-to-peak, and the amplitude was unrelated to stride frequency. Yaw movements were larger due to spontaneous voluntary head shifts, and were smaller at higher walking velocities. Head translations were small (4 cm). Cynomolgus monkeys positioned their heads more forward in pitch than the rhesus monkeys. None of the animals maintained a forward head fixation point (HFP), indicating that the lVCR contributed little to compensatory head movements in these experiments. Significantly, aVCR gains in roll and pitch were close to unity and phases were 180º over the full frequency range of natural walking, which is in contrast to previous findings using anesthesia or passive trunk rotation with body restraint. We conclude that the behavioral state associated with active body motion is necessary to maintain head stability in pitch and roll over the full range of stride/step frequencies encountered during walking.