An emerging branch of social cognitive neuroscience attempts to unravel the critical cognitive mechanisms that enable humans to engage in joint action. In the current experiment, differences in brain activity in participants engaging in solitary action and joint action were identified using whole brain fMRI while participants performed a virtual bar-balancing task either alone ( S), or with the help of a partner in each of two separate joint-action conditions (isomorphic [ J i] and non-isomorphic [ J n]). Compared to the performing the task alone, BOLD signal was found to be stronger in both joint-action conditions at specific sites in the human mirror system (MNS). This activation pattern may reflect the demand on participants to simulate the actions of others, integrate their own actions with those of their partners, and compute appropriate responses. Increasing inter-dependence (complementarity) of movements being generated by cooperating individuals ( J n > J i > S) was found to correlate with BOLD signal in the right anterior node of the MNS (pars opercularis), and the area around the right temporoparietal junction (TPJ). These data are relevant to current debates concerning the role of right IFG in complementary action, as well as evolving theories of joint action.