Recent work on the model fly Drosophila melanogaster has reported inconsistencies in that they either do or do not prefer to lay eggs on intermediate concentrations of ethanol. We resolve this discrepancy by showing that this species strongly prefers ovipositing on ethanol when it is close to a non-ethanol substrate, but strongly avoids ethanol when options are farther apart. We also show fluidity of these behaviors among other Drosophila species: D. melanogaster is more responsive to ethanol than close relatives in that it prefers ethanol more than other species in the close-proximity case, but avoids ethanol more than other species in the distant case. In the close-proximity scenario, the more ethanol-tolerant species generally prefer ethanol more, with the exception of the island endemic D. santomea. This species has the lowest tolerance in the clade, but behaves like D. melanogaster. We speculate that this could be an adaptation to protect eggs from parasites or predators such as parasitoid wasps, as larvae migrate to non-toxic substrates after hatching. Here we use D. melanogaster to dissect the genetic basis of oviposition behavior specifically in the close-proximity case. We identified two QTL using inbred lines from the Drosophila Synthetic Population Resource. These loci map to the telomeric end of chromosome 2 and to the centrosome on chromosome 3. With continued fine mapping using introgression lines, we hope to narrow down the behavior to a few candidate genes. These natural differences both among and within species are an excellent opportunity to study how genes and brains evolve to alter ethanol preferences, and provide an interesting model for genetic variation in preferences in other organisms including humans.