The amygdala responds to emotional stimuli but habituates at repeated presentation. Much less is known about time-on-task effects during exposure to emotional stimuli in the cortex. Here, we identified the neural substrates that show habituation or cortical decreased activity in a task of repeated passive exposure to faces with negative emotional expressions. We found that in the amygdala, habituation selectively involved the central nucleus and extended posteriorly in the hippocampal-amygdaloid region, consistently with reduced motivational and attentional effects of repeated stimulation. In the cortex, decreases in activity with time on task involved a network including the temporoparietal junction, the postsplenial region, and the ventromedial prefrontal cortex, mostly located at the transition from task activations to deactivations. These effects were analogous to those reported as encoding of social cognition information, suggesting a role in developing task-based representations of input content.