During walking, the vestibular influence on locomotor activity is phase-dependent and modulated in both limbs with changes in velocity. It is unclear, however, whether this bilateral modulation is due to a coordinated mechanism between both limbs or instead through limb-specific processes that remain masked by the symmetric nature of locomotion. Here, human subjects walked on a split-belt treadmill with one belt moving at 0.4 m s−1 and the other moving at 0.8 m s−1 while exposed to an electrical vestibular stimulus. Muscle activity was recorded bilaterally around the ankles of each limb and used to compare vestibulo-muscular coupling between velocity-matched and unmatched tied-belt walking. In general, response magnitudes decreased by ∼20–50% and occurred ∼13–20% earlier in the stride cycle at the higher belt velocity. This velocity-dependent modulation of vestibular-evoked muscle activity was retained during split-belt walking and was similar within each limb to velocity-matched tied-belt walking. These results demonstrate that the vestibular influence on ankle muscles during locomotion can be adapted independently to each limb. Furthermore, modulation of vestibular-evoked muscle responses occurred rapidly (∼13–34 strides) after onset of split-belt walking. This rapid adaptation contrasted the prolonged adaptation in step length symmetry (∼128 strides) as well as EMG magnitude and timing (∼40–100 and ∼20–80 strides, respectively). These results suggest that vestibular influence on ankle muscle control is adjusted rapidly in sensorimotor control loops as opposed to longer-term error correction mechanisms commonly associated split-belt adaptation. Rapid limb-specific sensorimotor feedback adaptation may be advantageous for asymmetric overground locomotion, such as navigating irregular terrain or turning.