The brainstem locus coeruleus (LC) is a major source of noradrenaline to the forebrain and plays important roles in emotional learning. Though the LC receives synaptic inputs from the medial prefrontal cortex, a brain region important in cognitive and emotional processing, it is unclear whether and how prefrontal regions influence the LC particularly during fear extinction learning. To address this question, we first examined the detailed anatomical connectivity from prefrontal subregions to the LC in rats. Retrograde and anterograde tracing experiments showed that LC noradrenergic neurons receive monosynaptic projections from the prelimbic (PL) and infralimbic (IL) subregions of medial prefrontal cortex with topographically distinct axon distributions. Using optogenetic techniques, we next asked whether the PL and IL inputs to the LC participate in extinguishing auditory fear memories. Optogenetic terminal inactivation revealed that the IL-to-LC circuit is necessary for formation of long-term extinction memories, while the PL-to-LC pathway functions to resist fear memory extinction. Finally, using fiber photometry, we revealed distinct calcium dynamics in PL-to-LC and IL-to-LC input neurons during fear extinction learning. Both PL-to-LC and IL-to-LC inputs showed excitatory responses to the fear-conditioned tone, but their activity dynamics during extinction learning diverged. Specifically, IL-to-LC input neurons had sustained calcium increases in response to the conditioned tone through extinction learning, while PL-to-LC input neurons were activated during sensory triggered and internally generated aversive states. Together, our findings demonstrate that prefrontal subregions bidirectionally regulate fear extinction through differential modulation of the LC-noradrenaline system in a state-dependent manner.