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ABSTRACT While there is abundant theoretical work on the evolution of phenotype plasticity, empirical support has lagged. One model for the evolution of phenotype plasticity is by genetic accommodation. Under this model of evolution, when a population encounters a new environment there are widely variable responses among different genotypes, which are then pruned by selection into a single adaptive response. Because of the requirement to replicate genotypes, testing this prediction requires inbred lines as well as populations that are both adapted and not adapted to a resource. We previously demonstrated thatD. melanogasteradapted to ethanol through genetic accommodation usingD. simulansas an ancestral proxy lineage. However, we wondered how generalizable these results were. Here, we used a new population ofD. melanogasterfrom France and an ancestral range population from Zambia and measured behavioral tolerance to ethanol exposure in multiple genotypes from each population, as well as genome‐wide gene expression and alternative splicing in response to ethanol using RNA sequencing. We found that the ZambianD. melanogasterhave lower tolerance to ethanol than the FrenchD. melanogaster, with the Zambian flies becoming sedated while the French flies remain active under the same exposure. At the transcriptional level, Zambian genotypes showed extensive genotype‐specific changes in gene expression and splicing in response to ethanol exposure, while the French genotypes showed relatively modest and fewer genotype‐specific changes, consistent with having a more uniform, population response. We also found that gene expression and splicing appear to evolve independently of one another and that the splicing response to ethanol is largely distinct between populations. Thus, we have independently replicated evidence for evolution by genetic accommodation inD. melanogaster, suggesting that the evolution of plasticity may be an important contributor to the ability to exploit novel resources.