Light is a powerful environmental regulator of insect behavior. My thesis focuses on novel phototransduction mechanisms in insect central brain neurons that directly regulate physiology and behavior, independent of external eyes. I hypothesized that novel short wavelength-activated phototransduction mechanisms modulate complex behaviors such as arousal and decision-making. To test this, I developed and integrated molecular, electrophysiological, imaging, and behavioral approaches. I described mechanisms of a direct neuronal blue- and UV-light sensor, CRYPTOCHROME (CRY), in mediating behavioral responses to short wavelength light, and how CRY couples to membrane voltage-gated K+ β subunits, HYPERKINETIC. I also found that the previously uncharacterized Rhodopsin7 is a direct photoreceptor uniquely expressed in circadian neurons mediating circadian photoentrainment. I developed several assays to measure light-evoked avoidance/attraction behaviors with high spatial and temporal resolution in flies and mosquitoes. I demonstrated circadian regulation of these behaviors in Drosophila at the genetic and neuronal circuitry level. I also show valence control of light-evoked behavioral responses by integration of different light inputs, where nocturnal and diurnal mosquito species have unique, circadian clock-controlled behavioral preference to different light environments. Further, I identified that circadian neural circuits in the same mosquito species show striking anatomical and transcriptional diversities, which likely underlie observed behavioral differences. I conclude that light is a powerful cue that drives complex insect behaviors.