Humans automatically imitate other people’s actions during social interactions, building rapport and social closeness in the process. Although the behavioral consequences and neural correlates of imitation have been studied extensively, little is known about the neural mechanisms that control imitative tendencies. For example, the degree to which an agent is perceived as human-like influences automatic imitation, but it is not known how perception of animacy influences brain circuits that control imitation. In the current fMRI study, we examined how the perception and belief of animacy influence the control of automatic imitation. Using an imitation–inhibition paradigm that involves suppressing the tendency to imitate an observed action, we manipulated both bottom–up (visual input) and top–down (belief) cues to animacy. Results show divergent patterns of behavioral and neural responses. Behavioral analyses show that automatic imitation is equivalent when one or both cues to animacy are present but reduces when both are absent. By contrast, right TPJ showed sensitivity to the presence of both animacy cues. Thus, we demonstrate that right TPJ is biologically tuned to control imitative tendencies when the observed agent both looks like and is believed to be human. The results suggest that right TPJ may be involved in a specialized capacity to control automatic imitation of human agents, rather than a universal process of conflict management, which would be more consistent with generalist theories of imitative control. Evidence for specialized neural circuitry that “controls” imitation offers new insight into developmental disorders that involve atypical processing of social information, such as autism spectrum disorders.