Animals must constantly scan their environment for imminent threats to their safety. However, they must also integrate their past experiences across long timescales to assess the potential recurrence of new threats. Though visual inputs are critical for the detection of environmental danger, whether and how visual information shapes an animal's assessment of whether a new threat is likely to reappear in a given context is unknown. Using a novel behavioral assessment of long-term threat avoidance behavior, we find that animals will avoid a familiar location where they previously experienced a single exposure to an innately threatening visual stimulus. This avoidance behavior is highly sensitive and lasts for multiple days. Intriguingly, we find that the melanopsin-expressing, intrinsically photosensitive retinal ganglion cells tune this behavior via a perihabenular-nucleus accumbens circuit distinct from the canonical visual threat detection circuits. These findings define a specific retinal cell type driving a new long-term threat avoidance behavior driven by prior visual experience.