The ability to control and adapt joint stiffness is essential in human motor control. Both control loops on the spinal as well as cortical level are likely to play a role in this regulation. However, the cortical mechanisms involved with the online adaptive control of joint stiffness remain largely unresolved. This study aimed at identifying cortical areas associated with the process of joint stiffness modulation using electroencephalography (EEG). EEG was recorded in twelve healthy right-handed individuals performing an active posture control task while receiving continuous random force perturbations applied using a robotic manipulator. To provoke a change in the neuromuscular control strategy, i.e. adaptation of joint stiffness, external viscous loads were applied or removed between tasks or instantaneously within tasks. Linear time-invariant system identification techniques were used to estimate joint stiffness between tasks. Cortical oscillatory dynamics were analysed for eight clusters of independent components, which were found using independent component analysis (ICA) and a subsequent dipole source localization method. Power spectral analysis of the time-invariant trials revealed significant enhancement of theta and beta oscillations in the left sensorimotor cortex (S1/M1) and suppression of delta rhythms in the supplementary motor area (SMA) when external damping was present. Analysis of event-related spectral perturbations (ERSPs) in the time-variant trials revealed delta and theta band enhancement in the SMA and sensorimotor cortex following immediately after external damping removal, as well as broadband enhancement in the prefrontal cortex (anterior cingulate cortex (ACC)). Moreover, we found more pronounced modulations in cortical activity with an unexpected decrease in external damping as compared to an increase in viscous loads. These results suggest that multiple cortical areas are likely to be involved in modulating joint stiffness when stability is at risk being the sensorimotor cortex, SMA and prefrontal cortex, whereas adaptive processes in response to increased stability margins might be regulated on a subcortical level.