Humans cannot help but attribute human emotions to non-human animals. Although such attributions are often regarded as gratuitous anthropomorphisms and held apart from the attributions humans make about each other’s internal states, they may be the product of a general mechanism for flexibly interpreting adaptive behavior. To examine this, we used functional magnetic resonance imaging (fMRI) in humans to compare the neural mechanisms associated with attributing emotions to humans and non-human animal behavior. Although undergoing fMRI, participants first passively observed the facial displays of human, non-human primate and domestic dogs, and subsequently judged the acceptability of emotional (e.g. ‘annoyed’) and facial descriptions (e.g. ‘baring teeth’) for the same images. For all targets, emotion attributions selectively activated regions in prefrontal and anterior temporal cortices associated with causal explanation in prior studies. These regions were similarly activated by both human and non-human targets even during the passive observation task; moreover, the degree of neural similarity was dependent on participants’ self-reported beliefs in the mental capacities of non-human animals. These results encourage a non-anthropocentric view of emotion understanding, one that treats the idea that animals have emotions as no more gratuitous than the idea that humans other than ourselves do.