Vestibular input has been implicated to provide idiothetic cues for spatial navigation. It remains unresolved as to whether GABAergic synapses in the vestibular nucleus (VN) during a postnatal critical period regulates the acquisition of spatial recognition. To assess the role of GABAergic VN transmission on the acquisition of spatial navigation, we implanted above the VN of postnatal day 1 (P1) rats with a slice of Elvax loaded with GABAA receptor agonist (muscimol) or antagonist (bicuculline). These pups were allowed to recover and were tested for either activity-dependent plasticity of GABAergic synapses in the developing VN or for navigation test at the adult stage. First, whole-cell patch clamp recordings were conducted in brainstem slices. In normal animals, theta-burst stimulation delivered to vestibular afferents could induce long-term depression of GABAA receptor-mediated evoked-IPSCs (iLTD) in VN neurons of P7 rats but these responses became hardly inducible by P14. In rats pretreated with muscimol at P1, iLTD observable at P7 was abolished. In rats pretreated with bicuculline at P1, the emergence of iLTD was delayed to P9-14. To assess the impact of these GABAergic responses on the acquisition of spatial navigation, a path integration task (viz. dead reckoning) that primarily relies on sensory cues from vestibular organ was used. When compared with the sham controls, rats pretreated with muscimol at P1 showed no significant difference in light, dark, and new location probe tests. However, pretreatment with bicuculline at P1 significantly prolonged the training days, searching time, returning time, heading angle, and number of errors in both dark and new location probe tests. Taken together, we have provided evidence that the efficacy of GABAergic synapses in the developing VN constitutes a crucial component required for the expression of spatial navigation behavior in adults.