V6 is a retinotopic area located in the dorsal visual stream that integrates eye movements with retinal and visuo-motor signals. Despite the known role of V6 in visual motion, it is unknown whether it is involved in navigation and how sensory experiences shape its functional properties. We explored the involvement of V6 in egocentric navigation in sighted and in congenitally blind (CB) participants navigating via an in-house distance-to-sound sensory substitution device (SSD), the EyeCane. We performed two fMRI experiments on two independent datasets. In the first experiment, CB and sighted participants navigated the same mazes. The sighted performed the mazes via vision, while the CB via audition. The CB performed the mazes before and after a training session using the EyeCane SSD. In a second experiment a group of sighted people performed a motor topography task. Our results show that right V6 (rhV6) is selectively involved in egocentric navigation independently of the sensory modality used. Indeed, after training, rhV6 of CB is selectively recruited for auditory navigation, similar to rhV6 in the sighted. Moreover, we found activation for body movement in area V6, that can putatively contribute to its involvement in egocentric navigation. Taken together, our findings suggest that area rhV6 is a unique hub that transforms spatially relevant sensory information into an egocentric representation for navigation. While vision is clearly the dominant modality, rhV6 is in fact a supramodal area that can develop its selectivity for navigation in the absence of visual experience.