The term 'vestibular compensation' refers to the resolution of motor deficits resulting from a peripheral vestibular lesion. We investigated the role of the cerebellum in the compensation process, by characterizing the vestibulo-ocular reflex (VOR) evoked by head rotations at frequencies and velocities similar to those in natural behaviors in wild-type (WT) versus cerebellar-deficient Lurcher (Lc/+) mice. We found that during exploratory activity, normal mice produce head rotations largely consisting of frequencies up to 4Hz and velocities and accelerations as large as 400°/s² and 5000°/s², respectively. Accordingly, the VOR was characterized using sinusoidal rotations (0.2-4Hz) as well as transient impulses (~400°/s²; ~2,000/s²). Before lesions, WT and Lc/+ mice produced similar VOR responses to sinusoidal rotation. Lc/+ mice, however, had significantly reduced gains for transient stimuli. After unilateral labyrinthectomy, VOR recovery followed a similar course for WT and Lc/+ groups during the first week: gain was reduced by 80% for ipsilesionally-directed head rotations on day 1 and improved for both strains to values of ~0.4 by day 5. Moreover, responses evoked by contralesionally directed rotations returned to pre-lesion in both strains within this period. However, unlike WT which showed improving responses to ipsilesionally-directed rotations, recovery plateaued after first week for Lc/+ mice. Our results show that despite nearly normal recovery in the acute phase, long-term compensation is compromised in Lc/+. We conclude that cerebellar pathways are critical for long-term restoration of VOR during head rotation toward the lesioned side, while non-cerebellar pathways are sufficient to restore proper gaze stabilization during contralesionally-directed movements.