Brief smooth eye-velocity responses to target position steps have been reported during smooth pursuit. We investigated position-error responses in eight healthy human subjects, comparing the effects of a step-ramp change in target position when imposed upon steady-state smooth pursuit, vestibulo-ocular reflex (VOR) slow phases, or fixation. During steady-state pursuit or VOR, the target performed a step-ramp movement in the same or in the opposite direction relative to ongoing eye movements. When the step was directed backward relative to steady-state smooth pursuit, eye velocity transiently decreased (1.3 ± 0.4°/s; average peak change in amplitude ± SD), beginning ~100ms after the step. The amplitude of position-error responses varied inversely with step size. In contrast, there was little or no response in trials with forward steps during steady-state smooth pursuit, when step-ramps were imposed on VOR or when smooth pursuit began from fixation. We hypothesize that during ongoing smooth tracking when a sudden shift in target position is detected the pursuit system compares the direction of ongoing eye velocity with the relative positional error on the retina. In case of different relative directions between ongoing tracking and a new target eccentricity, a position-error response towards the new target is initiated. Such a mechanism might help the smooth pursuit system to respond better to changes in target direction. These experimental findings were simulated by a mathematical model of smooth pursuit by implementing direction-dependent behavior with a position-error gating mechanism.