The vestibular system plays a pivotal role in tracking head direction for effective navigation in complex environments. We hypothesize that the decline in navigational ability observed with aging is closely linked to the deterioration of a key ascending vestibular pathway in the head-direction network. With cre-dependent viruses for both anterograde and retrograde tracings, we discovered in mice a previously unreported direct pathway from the medial vestibular nucleus (MVN) to the dorsal tegmental nucleus (DTN), supplementing the conventional indirect pathways via the nucleus prepositus hypoglossi and/or the supragenual nucleus. Furthermore, optogenetics-assisted in vitro electrophyiological recording confirmed that this MVN-DTN pathway was monosynaptic and excitatory in nature. Through pathway-specific in vivo chemogenetics and navigational behavior tests, we demonstrated that selective silencing of this MVN-DTN pathway disrupted navigation behavior in adult mice. Additionally, our results in aged mice revealed a reduction in synaptic connectivity between MVN and DTN, as evidenced by synaptophysin tagging and in vitro whole-cell patch-clamp recording. This reduction was shown to play a functional role in the decline of homing ability during active navigation in aged mice. Overall, our study provides valuable insights into the intricacies of the vestibular system and its impact on spatial cognition with aging. These findings have the potential to inform the development of innovative therapeutic interventions aimed at improving spatial cognition in the aging population.