Acute peripheral vestibulopathy, also known as vestibular neuritis, causes disabling vertigo, nausea, vomiting, and imbalance. Although spontaneous recovery occurs, many individuals are left with persistent symptoms that interfere with everyday function. There are no medications that restore vestibular function; instead, patients are referred for vestibular rehabilitation. Vestibular therapy seeks to facilitate normal motor learning to improve balance and gaze stability. Although effective, standard home vestibular exercises are not engaging, are difficult to customize precisely to a patient’s individual level of impairment, and are not easily tracked to assess adherence. Virtual reality and computer gaming have the potential to address these limitations. We developed a custom computer game to deliver calibrated visual-vestibular mismatch and tested its ability to induce motor learning in the intact vestibulo-ocular reflex (VOR), with and without an incremental gain algorithm. Playing this game for approximately 30 min (300 VOR trials) with 50% increased visual demand led to a robust VOR gain increase of about 15% (30% of demand), for both incremental and non-incremental training. All participants tolerated the game experience well. These results support the further development of this game-based approach for clinical vestibular rehabilitation.