Vestibular input is required for accurate locomotion in the dark yet blind subjects’ vestibular function is unexplored. Such investigation may also identify visually-dependent aspects of vestibular function. We assessed vestibular function perceptually in six congenitally blind (and twelve sighted) subjects. Cupula deflection by a transient angular, horizontal acceleration generates a related vestibular nerve signal that declines exponentially with time constant 4-7s which is prolonged to 15s in the evoked vestibular-ocular reflex by the brainstem ‘velocity storage’. We measured perceptual velocity storage in blind subjects following velocity steps (overall perceptual vestibular time constant, Experiment 1) and found it to be significantly shorter (5.34s; range 2.39--8.58s) than in control sighted subjects (15.8s; P<0.001). Vestibular navigation was assessed by subjects steering a motorised Barany-chair in response to imposed angular displacements in a path-reversal task, ‘Go-Back-to-Start’ (GBS:Experiment 2); and a path-completion task, ‘Complete-the-Circle’ (CTC:Experiment 3). GBS performances (comparing response vs stimulus displacement regression slopes and r2) were equal between groups (P>0.05) but the Blind showed worse CTC performance (P<0.05). Two blind individuals showed ultrashort perceptual time constants, high lifetime physical activity scores and superior CTC performances; we speculate that these factors may be inter-related. In summary, the vestibular velocity storage as measured perceptually, is visually dependent. Early blindness does not affect path reversal performance but is associated with worse path completion, a task requiring an absolute spatial strategy. Although congenitally blind subjects are overall less able to utilize spatial mechanisms during vestibular navigation, prior extensive physical spatial activity may enhance vestibular navigation.