Humans possess efficient mechanisms to behave adaptively in social contexts. They ascribe goals and beliefs to others and use these for behavioural predictions. Researchers argued for two separate mental attribution systems: an implicit and automatic one involved in online interactions, and an explicit one mainly used in offline deliberations. However, the underlying mechanisms of these systems and the types of beliefs represented in the implicit system are still unclear. Using neuroimaging methods, we show that the right temporo-parietal junction and the medial prefrontal cortex, brain regions consistently found to be involved in explicit mental state reasoning, are also recruited by spontaneous belief tracking. While the medial prefrontal cortex was more active when both the participant and another agent believed an object to be at a specific location, the right temporo-parietal junction was selectively activated during tracking the false beliefs of another agent about the presence, but not the absence of objects. While humans can explicitly attribute to a conspecific any possible belief they themselves can entertain, implicit belief tracking seems to be restricted to beliefs with specific contents, a content selectivity that may reflect a crucial functional characteristic and signature property of implicit belief attribution.