The parietal-eye photoreceptor is unique because it has two antagonistic light signaling pathways in the same cell-a hyperpolarizing pathway maximally sensitive to blue light and a depolarizing pathway maximally sensitive to green light. Here, we report the molecular components of these two pathways. We found two opsins in the same cell: the blue-sensitive pinopsin and a previously unidentified green-sensitive opsin, which we name parietopsin. Signaling components included gustducin-α and Gαo, but not rod or cone transducin-α. Single-cell recordings demonstrated that Go mediates the depolarizing response. Gustducin-α resembles transducin-α functionally and likely mediates the hyperpolarizing response. The parietopsin-Go signaling pair provides clues about how rod and cone phototransduction might have evolved.