The thalamus receives input from multiple brain systems and has an essential role in controlling brain state. This is thought to occur primarily because of its connectivity with the forebrain. Here, we provide evidence for an additional mechanism. By calcium imaging of larval zebrafish, we show that two stimuli, light and darkness, trigger distinct activity patterns in the habenula. Responses appear first in a neuropil that is innervated by retino-recipient thalamic nuclei. Thalamic responses to light and darkness resemble habenula responses, and the thalamus appears to be the only source of GABAergic afferents that would underlie the inhibitory component of light-evoked activity. These data establish that the thalamus directly controls the habenula, a regulator of many broadly acting neuromodulators. We thus propose that the thalamus influences brain state via a pathway to the habenula, which can act in parallel with projections to the forebrain.