Small insects regulate their body temperature solely through behavior. Thus, sensing environmental temperature and implementing an appropriate behavioral strategy can be critical for survival. The fly Drosophila melanogaster prefers 24 degrees C, avoiding higher and lower temperatures when tested on a temperature gradient. Furthermore, temperatures above 24 degrees C have negative reinforcing properties. In contrast, we found that flies have a preference in operant learning experiments for a low-temperature-associated position rather than the 24 degrees C alternative in the heat-box. Two additional differences between high- and low-temperature reinforcement, i.e., temperatures above and below 24 degrees C, were found. Temperatures equally above and below 24 degrees C did not reinforce equally and only high temperatures supported increased memory performance with reversal conditioning. Finally, low- and high-temperature reinforced memories are similarly sensitive to two genetic mutations. Together these results indicate the qualitative meaning of temperatures below 24 degrees C depends on the dynamics of the temperatures encountered and that the reinforcing effects of these temperatures depend on at least some common genetic components. Conceptualizing these results using the Wolf-Heisenberg model of operant conditioning, we propose the maximum difference in experienced temperatures determines the magnitude of the reinforcement input to a conditioning circuit.