Alcohol activates reward systems through an unknown mechanism, in some cases leading to alcohol abuse and dependence. Herein, we utilized a two-choice Capillary Feeder assay to address the neural and molecular basis for ethanol self-administration in Drosophila melanogaster. Wild-type Drosophila shows a significant preference for food containing between 5% and 15% ethanol. Preferred ethanol self-administration does not appear to be due to caloric advantage, nor due to perceptual biases, suggesting a hedonic bias for ethanol exists in Drosophila. Interestingly, rutabaga adenylyl cyclase expression within intrinsic mushroom body neurons is necessary for robust ethanol self-administration. The expression of rutabaga in mushroom bodies is also required for both appetitive and aversive olfactory associative memories, suggesting that reinforced behavior has an important role in the ethanol self-administration in Drosophila. However, rutabaga expression is required more broadly within the mushroom bodies for the preference for ethanol-containing food than for olfactory memories reinforced by sugar reward. Together these data implicate cAMP signaling and behavioral reinforcement for preferred ethanol self-administration in D. melanogaster.