Visually induced self-motion perception (vection) relies on visual-vestibular interaction. Imaging studies using vestibular stimulation have revealed a vestibular thalamo-cortical dominance in the right hemisphere in right handers and the left hemisphere in left handers. We investigated if the behavioural characteristics and neural correlates of vection differ between healthy left and right-handed individuals. 64-channel EEG was recorded while 25 right handers and 25 left handers were exposed to vection-compatible roll motion (coherent motion) and a matched, control condition (incoherent motion). Behavioural characteristics, i.e. vection presence, onset latency, duration and subjective strength, were also recorded. The behavioural characteristics of vection did not differ between left and right handers (all p > 0.05). Fast Fourier Transform (FFT) analysis revealed significant decreases in alpha power during vection-compatible roll motion (p < 0.05). The topography of this decrease was handedness-dependent, with left handers showing a left lateralized centro-parietal decrease and right handers showing a bilateral midline centro-parietal decrease. Further time-frequency analysis, time locked to vection onset, revealed a comparable decrease in alpha power around vection onset and a relative increase in alpha power during ongoing vection, for left and right handers. No effects were observed in theta and beta bands. Left and right-handed individuals show vection-related alpha power decreases at different topographical regions, possibly related to the influence of handedness-dependent vestibular dominance in the visual-vestibular interaction that facilitates visual self-motion perception. Despite this difference in where vection-related activity is observed, left and right handers demonstrate comparable perception and underlying alpha band changes during vection.