Vestibular neuritis (VN) is a sudden peripheral unilateral vestibular failure with often persistent head movement-related dizziness and unsteadiness. Compensation of asymmetrical activity in the primary peripheral vestibular afferents is accomplished by restoration of impaired brainstem vestibulo-ocular and vestibulo-spinal reflexes, but presumably also by changing cortical vestibular tone imbalance subserving, e.g., spatial perception and orientation. The aim of this study was to elucidate (i) whether there are changes of cerebral resting-state networks with respect to functional interregional connectivity (resting-state activity) in VN patients and (ii) whether these are related to neurophysiological, perceptual and functional parameters of vestibular-induced disability. Using independent component analysis (ICA), we compared resting-state networks between 20 patients with unilateral VN and 20 age- and gender-matched healthy control subjects. Patients were examined in the acute VN stage and after 3 months. A neural network (component 50) comprising the parietal lobe, medial aspect of the superior parietal lobule, posterior cingulate cortex, middle frontal gyrus, middle temporal gyrus, parahippocampal gyrus, anterior cingulate cortex, insular cortex, caudate nucleus, thalamus and midbrain was modulated between acute VN patients and healthy controls and in patients over time. Within this network, acute VN patients showed decreased resting-state activity (ICA) in the contralateral intraparietal sulcus (IPS), in close vicinity to the supramarginal gyrus (SMG), which increased after 3 months. Resting-state activity in IPS tended to increase over 3 months in VN patients who improved with respect to functional parameters of vestibular-induced disability (VADL). Resting-state activity in the IPS was not related to perceptual (subjective visual vertical) or neurophysiological parameters of vestibular-induced disability (e.g., gain of vestibulo-ocular reflex, caloric responsiveness, postural sway). VN leads to a change in resting-state activity of the contralateral IPS adjacent to the SMG, which reverses during vestibular compensation over 3 months. The ventral intraparietal area in the IPS contains multimodal regions with directionally selective responses to vestibular stimuli making them suitable for participating in spatial orientation and multisensory integration. The clinical importance is indicated by the fact that the increase in resting-state activity tended to be larger in those patients with only little disability at the follow-up examination. This may indicate powerful restitution-related or compensatory cortical changes in resting-state activity.