Context facilitates the recognition of forthcoming actions by pointing to which intention is likely to drive them. This intention is thought to be estimated in a ventral pathway linking MTG with frontal regions and to further impact on the implementation of sensory predictions within the action observation network (AON). Additionally, when conflicting intentions are estimated from context, the DLPFC may bias action selection. However, direct evidence for the contribution of these areas to context-embedded action representations in the AON is still lacking. Here, we used a perturb-and-measure TMS-approach to disrupt neural activity, separately in MTG and DLPFC and subsequently measure cortico-spinal excitability while observing actions embedded in congruent, incongruent or ambiguous contexts. Context congruency was manipulated in terms of compatibility between observed kinematics and the action goal suggested by the ensemble of objects depicted in the environment. In the control session (vertex), we found an early facilitation and later inhibition for kinematics embedded in congruent and incongruent contexts, respectively. MTG stimulation altered the differential modulation of M1 response to congruent vs. incongruent contexts, suggesting this area specifies prior representations about appropriate object graspability. Interestingly, all effects were abolished after DLPFC stimulation highlighting its critical role in broader contextual modulation of the AON activity.