The concept of auditory–motor interaction pervades speech science research, yet the cortical systems supporting this interface have not been elucidated. Drawing on experimental designs used in recent work in sensory–motor integration in the cortical visual system, we used fMRI in an effort to identify human auditory regions with both sensory and motor response properties, analogous to single-unit responses in known visuomotor integration areas. The sensory phase of the task involved listening to speech (nonsense sentences) or music (novel piano melodies); the “motor” phase of the task involved covert rehearsal/humming of the auditory stimuli. A small set of areas in the superior temporal and temporal– parietal cortex responded both during the listening phase and the rehearsal/humming phase. A left lateralized region in the posterior Sylvian fissure at the parietal–temporal boundary, area Spt, showed particularly robust responses to both phases of the task. Frontal areas also showed combined auditory + rehearsal responsivity consistent with the claim that the posterior activations are part of a larger auditory–motor integration circuit. We hypothesize that this circuit plays an important role in speech development as part of the network that enables acoustic–phonetic input to guide the acquisition of language-specific articulatory-phonetic gestures; this circuit may play a role in analogous musical abilities. In the adult, this system continues to support aspects of speech production, and, we suggest, supports verbal working memory.