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The ability to survive within a cooperative society depends on impartial third-party punishment (TPP) of social norm violations. Two cognitive mechanisms have been postulated as necessary for the successful completion of TPP: evaluation of legal responsibility and selection of a suitable punishment given the magnitude of the crime. Converging neuroimaging research suggests two supporting domain-general networks; a mentalizing network for evaluation of legal responsibility and a central-executive network for determination of punishment. A whole-brain voxel-based lesion-symptom mapping approach was used in conjunction with a rank-order TPP task to identify brain regions necessary for TPP in a large sample of patients with penetrating traumatic brain injury. Patients who demonstrated atypical TPP had specific lesions in core regions of the mentalizing (dorsomedial prefrontal cortex [PFC], ventromedial PFC) and central-executive (bilateral dorsolateral PFC, right intraparietal sulcus) networks. Altruism and executive functioning (concept formation skills) were significant predictors of TPP: altruism was uniquely associated with TPP in patients with lesions in right dorsolateral PFC and executive functioning was uniquely associated with TPP in individuals with lesions in left PFC. Our findings contribute to the extant literature to support underlying neural networks associated with TPP, with specific brain-behavior causal relationships confirming recent functional neuroimaging research.