Almost all animals can sense light, but only those with spatial vision can ‘‘see.’’ Conventionally, this was restricted to animals possessing discrete visual organs (eyes), but extraocular vision could facilitate vision without eyes. Echinoderms form the focus of extraocular vision research [1–7], and the brittle star Ophiocoma wendtii, which exhibits light-responsive color change and shelter seeking, became a key species of interest [4, 8, 9]. Both O. wendtii and an apparently light-indifferent congeneric, O. pumila, possess an extensive network of r-opsin-reactive cells, but its function remains unclear . We show that, although both species are strongly light averse, O. wendtii orients to stimuli necessitating spatial vision for detection, but O. pumila does not. However, O. wendtii’s response disappears when chromatophores are contracted within the skeleton. Combining immunohistochemistry, histology, and synchrotron microtomography, we reconstructed models of photoreceptors in situ and extracted estimated angular apertures for O. wendtii and O. pumila. Angular sensitivity estimates, derived from these models, support the hypothesis that chromatophores constitute a screening mechanism in O. wendtii, providing sufficient resolving power to detect the stimuli. RNA sequencing (RNA-seq) identified opsin candidates in both species, including multiple r-opsins and transduction pathway constituents, congruent with immunohistochemistry and studies of other echinoderms [10, 11]. Finally, we note that differing body postures between the two species during experiments may reflect aspect of signal integration. This represents one of the most detailed mechanisms for extraocular vision yet proposed and draws interesting parallels with the only other confirmed extraocular visual system, that of some sea urchins, which also possess chromatophores.