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Brains likely evolved from diffuse nerve nets in the Precambrian, but we do not know what the first brains looked like or how they were organized. Acoel worms, the sister lineage to all other animals with brains, offer a window into this transition. We studied the three-banded panther worm Hofstenia miamia, whose brain is diffuse and unlike any previously described: it shows little anatomical or functional regionalization or stereotypy. Worms forage successfully even after large portions of the brain are removed, suggesting most regions can perform most computations. Neural cell type markers are also distributed across the brain with little regionalization. High-resolution studies of hunting reveal that more brain tissue improves performance, but no specific brain region is required. These results lead us to propose that H. miamia’s brain is built from computationally pluripotent ‘tiles’, whose interactions generate coherent behavior. This architecture suggests that early brains arose by condensation of diffuse nerve nets into unregionalized brains, with regionalization evolving secondarily.