The visual motion aftereffect (MAE) is the most prominent aftereffect in the visual system. Regarding its function, psychophysical studies suggest its function to be a form of sensory error correction, possibly also triggered by incongruent visual-vestibular stimulation. Several observational imaging experiments have deducted an essential role for region MT+ in the perception of a visual MAE but not provided conclusive evidence. Potential confounders with the MAE such as ocular motor performance, attention, and vection sensations have also never been controlled for. Aim of this neuroimaging study was to delineate the neural correlates of MAE and its subjacent functional connectivity pattern. A rotational MAE (n = 22) was induced using differing visual stimuli whilst modulating ocular motor parameters in a 3T scanner. Data was analyzed with SPM12. Eye movements as a response to the same stimuli were studied by means of high-resolution videooculography. Analysis for all stimuli gave bilateral activations along the dorsal visual stream with an emphasis on area MT. The onset of a visual MAE revealed an additional response in the right medial superior temporal area (MST) and a concurrent deactivation of vestibular hub region OP2. There was no correlation for the BOLD effects during the MAE with either ocular motor or attention parameters. The functional correlate of a visual MAE in humans may be represented in the interaction between region MT and area MST. This MAE representation is independent of a potential afternystagmus, attention and the presence of egomotion sensations. Connectivity analyses showed that in the event of conflicting visual-vestibular motion information (here MAE) area MST and area OP2 may act as the relevant mediating network hubs.