It is often necessary for individuals to coordinate their actions with others. In the real world, joint actions rely on the direct observation of co-actors and rhythmic cues. But how are joint actions coordinated when such cues are unavailable? To address this question, we recorded brain activity while pairs of participants guided a cursor to a target either individually (solo control) or together with a partner (joint control) from whom they were physically and visibly separated. Behavioural patterns revealed that joint action involved real-time coordination between co-actors and improved accuracy for the lower performing co-actor. Concurrent neural recordings and eye tracking revealed that joint control affected cognitive processing across multiple stages. Joint control involved increases in both behavioural and neural coupling – both quantified as interpersonal correlations – peaking at action completion. Correspondingly, a neural offset response acted as a mechanism for and marker of interpersonal neural coupling, underpinning successful joint actions.