Carbon dioxide is produced by many organic processes, and is a convenient volatile cue for insects searching for blood hosts, flowers, communal nests, fruit, and wildfires. Curiously, although Drosophila melanogaster feed on yeast that produce CO2 and ethanol during fermentation, laboratory experiments suggest that walking flies avoid CO2. Here, we resolve this paradox by showing that both flying and walking Drosophila find CO2 attractive, but only when in an active state associated with foraging. Aversion at low activity levels may be an adaptation to avoid CO2-seeking-parasites, or succumbing to respiratory acidosis in the presence of high concentrations of CO2 that exist in nature. In contrast to CO2, flies are attracted to ethanol in all behavioral states, and invest twice the time searching near ethanol compared to CO2. These behavioral differences reflect the fact that whereas CO2 is generated by many natural processes, ethanol is a unique signature of yeast fermentation. Using genetic tools, we determined that the evolutionarily ancient ionotropic co-receptor IR25a is required for CO2 attraction, and that the receptors necessary for CO2 avoidance are not involved. Our study lays the foundation for future research to determine the neural circuits underlying both state- and odorant- dependent decision making in Drosophila.