Optogenetic studies in mice have revealed new relationships between well-defined neurons and brain functions. However, there are currently no means to achieve the same cell-type specificity in monkeys, which possess an expanded behavioral repertoire and closer anatomical homology to humans. Here, we present a resource for cell-type-specific channelrhodopsin expression in Rhesus monkeys and apply this technique to modulate dopamine activity and monkey choice behavior. These data show that two viral vectors label dopamine neurons with greater than 95% specificity. Infected neurons were activated by light pulses, indicating functional expression. The addition of optical stimulation to reward outcomes promoted the learning of reward-predicting stimuli at the neuronal and behavioral level. Together, these results demonstrate the feasibility of effective and selective stimulation of dopamine neurons in non-human primates and a resource that could be applied to other cell types in the monkey brain. Display omitted •Cell-type-specific promoter drives Cre-dependent ChR2 expression in monkey•Optogenetically activated neurons had dopamine-like features and reward responses•Dopamine neurons respond strongly to cues predicting optical stimulation•Monkeys choose predicted optogenetic stimulation over no predicted stimulation Cell-type specific optogenetic stimulation in Rhesus monkeys allows manipulation of dopamine neurons to demonstrate their role in reward-based learning