The sleeping brain is in a constant tradeoff between maintaining its quiescent state, thought to support homeostatic processes, and interrupting it to deal with external contingencies such as threat. While evidence suggests that sleep interruption is an associative contextual process, little is known about its underlying neural substrates. Here, inspired by evidence that sleep interruption in humans relies on associative and contextual components, we develop a paradigm in mice to identify its circuit mechanisms. By training mice on an active avoidance task variant, we discover that auditory conditioning results in selective sleep interruption that is causally dependent on the amygdala. Electrophysiological recordings in task-performing mice reveal amygdala circuit reorganization following associative conditioning. By examining sleep interruption in different behavioral arenas, we find that mice also show contextual behavioral specificity, and that this process engages prefrontal cortex. Prefrontal inhibition reinstates sleep interruption in safe environments, along with the underlying amygdala transformation supporting it. Overall, our work shows a prefrontal to amygdala pathway for adaptive sleep interruption, extending the notion of top-down executive control to decision making during sleep.