Low-frequency sinusoidal galvanic vestibular stimulation (sGVS) can induce perceptions of sway and nausea through entraining vestibular afferent firing to the sinusoidal stimulus. As recently shown, concurrent dorsolateral prefrontal cortex (dlPFC) stimulation via transcranial alternating current stimulation (tACS) greatly attenuates these vestibular perceptions. Given that both vestibular afferents and dlPFC efferents project to the insular cortex, it was reasoned that the insula is the most likely area for the top-down inhibitory interaction to take place. To identify the sites of this interaction, blood-oxygen-level-dependent (BOLD) functional magnetic resonance imaging (fMRI) was collected whilst simultaneously delivering sinusoidal electrical stimulation (±2 mA, 0.2 Hz, 60 cycles) to 20 participants. These stimuli were randomly applied as follows: (i) bilateral sGVS alone via the mastoid processes; (ii) tACS of the dlPFC alone at electroencephalogram site F4; and (iii) sGVS and tACS together. Altered BOLD signal-intensity patterns were identified in the parieto-insular vestibular cortex and thalamus when comparing both sGVS and dlPFC stimulation to concurrent stimulation. Within the brainstem, signal-intensity increased in the inferior olivary nucleus and decreased in the nucleus of the solitary tract during concurrent stimulation, when analysed relative to single stimuli. Because concurrent stimulation elicited different activation patterns in each of these regions compared to the single stimuli, they were considered to be key for the interaction. Given the role each plays in dlPFC and vestibular pathways, the inhibitory function exerted by the dlPFC on vestibular processing likely involves ongoing modulation of one or several of these cortical centres.