Social interactions are not simply governed by the learned sensorimotor contingencies between action and outcome but are rather based on the ability to predict the hidden intentions or state of mind of others. Conversely, the inability to interact successfully can lead to interpersonal conflicts, economic loss and societal discord. Such deficits in interactive social behavior are also a prominent feature of many neurocognitive disorders, including major depression, schizophrenia and Autism Spectrum Disorder (ASD). Despite the immense importance of basic interactive social behavior to both normal and abnormal cognition, its single-neuronal basis and causal underpinnings remain almost completely unknown. While this level of investigation is not readily accessible in humans, non-human primates are a particularly suitable model for understanding basic elements of human social behavior, as their social cognition reflects the highest degree of sophistication known in the animal kingdom. In recent work, we discovered specific neurons in the primate dorsal anterior cingulate (dACC) that selectively predict an opponent’s yet unknown decision to invest in a common good or defect, and distinct neurons that encode the monkey’s own current decision based on prior outcomes. Mixed population predictions of the other was remarkably near-optimal compared to behavioral decoders. Moreover, disrupting cingulate activity selectively biased mutually beneficial interactions between monkeys but, surprisingly, had no influence on their decisions when no net-positive outcome was possible. Our findings identify and characterize groups of self-encoding and other-predictive neurons in the primate anterior cingulate essential for enacting cooperative interactions, and open the way towards developing targeted treatment of social behavioral disorders.