Cooperative action involves the simulation of actions and their co-representation by two or more people. This requires the involvement of two complex brain systems: the mirror neuron system (MNS) and the mentalizing system (MENT), both of critical importance for successful social interaction. However, their internal organization and the potential synergy of both systems during joint actions (JA) are yet to be determined. The aim of this study was to examine the role and interaction of these two fundamental systems-MENT and MNS-during continuous interaction. To this hand, we conducted a multiple-brain connectivity analysis in the source domain during a motor cooperation task using high-density EEG dual-recordings providing relevant insights into the roles of MNS and MENT at the intra- and interbrain levels. In particular, the intra-brain analysis demonstrated the essential function of both systems during JA, as well as the crucial role played by single brain regions of both neural mechanisms during cooperative activities. Specifically, our intra-brain analysis revealed that both neural mechanisms are essential during Joint Action (JA), showing a solid connection between MNS and MENT and a central role of the single brain regions of both mechanisms during cooperative actions. Additionally, our inter-brain study revealed increased inter-subject connections involving the motor system, MENT and MNS. Thus, our findings show a mutual influence between two interacting agents, based on synchronization of MNS and MENT systems. Our results actually encourage more research into the still-largely unknown realm of inter-brain dynamics and contribute to expand the body of knowledge in social neuroscience.