Adult ageing results in a progressive loss of vestibular hair cell receptors and afferent fibres. Given the robustness of vestibulo-ocular and vestibular-evoked whole-body responses to age-related deterioration, it was proposed that the vestibular system compensates centrally. Here we examine the potential for central compensation in vestibular sensitivity with adult ageing by using a combination of real and virtual rotation-based psychophysical testing at two stimulus frequencies (0.1 & 1 Hz). Real rotations activate semi-circular canal hair cell receptors naturally via mechanotransduction, while electrical current used to evoke virtual rotations does not rely on mechanical deformation of hair cell receptors to activate vestibular afferents. This two-pronged approach allows us to determine the independent effects of age-related peripheral afferent receptor loss and potential compensatory mechanisms. Older adults had thresholds for discriminating real rotations that were significantly greater than young adults at 0.1 Hz (7.2 vs. 3°/s), but the effect of age was weaker (non-significant) at 1 Hz (2.4 vs. 1.3°/s). For virtual rotations, older adults had greater thresholds than young adults at 0.1 Hz (1.2 vs. 0.5 mA), however, older adults outperformed young adults at 1 Hz (0.6 vs. 1.1 mA). Based on these thresholds, we argue that central vestibular processing gain is enhanced in older adults for 1 Hz real and virtual rotations, partially offsetting the negative impact of normal age-related hair cell receptor and primary afferent loss. We propose that the frequency dependence of this compensation reflects the physiological importance of the 1–5 Hz range in natural vestibular input.