Humans form social coalitions in every society on earth, yet we know very little about how the general concepts ‘us’ and ‘them’ are represented in the brain. Evolutionary psychologists have argued that the human capacity for group affiliation is a byproduct of adaptations that evolved for detecting more general coalitions. These theories suggest that humans possess a common neural code for the concepts ‘in-group’ and ‘out-group,’ regardless of the category by which group boundaries are instantiated. We used multivoxel pattern analysis to identify the neural substrates of generalized group concept representations. We trained a classifier to encode how people represented the most basic instantiation of a specific social group (i.e., arbitrary teams created in the lab with no history or associated stereotypes) and tested how well the neural data decoded membership along an objectively orthogonal, real-world category (i.e., political parties). The dorsal anterior cingulate cortex/middle cingulate cortex and anterior insula were associated with representing groups across multiple social categories. Restricting the analyses to these regions in a separate sample of participants performing an explicit categorization task, we replicated cross-categorization classification in anterior insula. Classification accuracy across categories was driven predominantly by the correct categorization of in-group targets, consistent with theories indicating in-group preference is more central than out-group derogation to group perception and cognition. These findings highlight the extent to which social group concepts rely on domain-general circuitry associated with encoding stimuli’s functional significance in service of responding adaptively to dynamic environments.