Most vertebrates process visual information using elaborately structured photosensory tissues, including the eyes and pineal. However, there is strong evidence that other tissues can detect and respond to photic stimuli [1–3]. Many reports suggest that photosensitive elements exist within the brain itself and inﬂuence physiology and behavior; however, a long-standing puzzle has been the identity of the neurons and photoreceptor molecules involved [4, 5]. We tested whether light cues inﬂuence behavior in zebraﬁsh larvae through deep brain photosensors. We found that larvae lacking eyes and pineal perform a simple light-seeking behavior triggered by loss of illumination (‘‘dark photokinesis’’). Neuroanatomical considerations prompted us to test orthopedia (otpa)-deﬁcient ﬁsh, which show a profound reduction in dark photokinesis. Using targeted genetic ablations, we narrowed the photosensitive region to neurons in the preoptic area. Neurons in this region express several photoreceptive molecules, but expression of the melanopsin opn4a is selectively lost in otpa mutants, suggesting that opn4a mediates dark photokinesis. Our ﬁndings shed light on the identity and function of deep brain photoreceptors and suggest that otpa speciﬁes an ancient population of sensory neurons that mediate behavioral responses to light.