Naked mole-rats (Heterocephalus glaber) form some of the most cooperative groups in the animal kingdom, living in multigenerational colonies under the control of a single breeding queen. Yet how they maintain this highly organized social structure is unknown. Here we show that the most common naked mole-rat vocalization, the soft chirp, is used to transmit information about group membership, creating distinctive colony dialects. Audio playback experiments demonstrate that individuals make preferential vocal responses to home colony dialects. Pups fostered in foreign colonies in early postnatal life learn the vocal dialect of their adoptive colonies, which suggests vertical transmission and flexibility of vocal signatures. Dialect integrity is partly controlled by the queen: Dialect cohesiveness decreases with queen loss and remerges only with the ascendance of a new queen.