Light exerts profound effects on cognitive functions across species, including humans. However, the neuronal mechanisms underlying the effects of light on cognitive functions are poorly understood. In this study, we show that long-term exposure to bright-light treatment promotes spatial memory through a di-synaptic visual circuit related to the nucleus reuniens (Re). Specifically, a subset of SMI-32-expressing ON-type retinal ganglion cells (RGCs) innervate CaMKIIα neurons in the thalamic ventral lateral geniculate nucleus and intergeniculate leaflet (vLGN/IGL), which in turn activate CaMKIIα neurons in the Re. Specific activation of vLGN/IGL-projecting RGCs, activation of Re-projecting vLGN/IGL neurons, or activation of postsynaptic Re neurons is sufficient to promote spatial memory. Furthermore, we demonstrate that the spatial-memory-promoting effects of light treatment are dependent on the activation of vLGN/IGL-projecting RGCs, Re-projecting vLGN/IGL neurons, and Re neurons. Our results reveal a dedicated subcortical visual circuit that mediates the spatial-memory-promoting effects of light treatment. Display omitted •Activation of Re-projecting vLGN/IGL neurons activates neuronal activity in the Re•SMI-32+ ON-type RGCs directly innervate the vLGN/IGL-Re pathway•Activation of the retina-vLGN/IGL-Re pathway promotes spatial memory•Light treatment promotes spatial memory via the retina-vLGN/IGL-Re pathway Huang et al. identified a visual circuit related to the Re that regulates spatial memory. They demonstrate that the retina-vLGN/IGL-Re pathway mediates the spatial-memory-promoting effects of light treatment.