Abstract It remains debated whether greater degrees of sexual dimorphism would evolve if not for intersexual genetic constraints. Here, we used experimental evolution to partially break the intersexual genetic constraint in Drosophila melanogaster to investigate the effects of a shared gene pool on the evolution of sexual dimorphism in gene expression. In six replicate populations of 1,000 flies, a dominant marker (DsRed) was used to force a “Red” pool of genetically variable Chromosome 2 copies through exclusive father-to-son inheritance, while a complimentary pool of “NonRed” chromosomes was inherited primarily from mothers to daughters. After 100 generations, we demonstrated the effect of Red male-limited chromosomes in increasing male mating success. Differentially expressed genes between flies with and without Red chromosomes had on average higher intersexual genetic correlations (rMF), as expected if such correlations represent a constraint to sex-specific adaptation under normal inheritance. If conflict hinders the evolution of further dimorphism, the transcriptomes of male-selected Red chromosomes were predicted to evolve to be “masculinized” relative to female-selected NonRed chromosomes. Consistent with this, splicing patterns in Red males (but not Red females) were masculinized relative to NonRed males. Contrastingly, gene expression levels were largely feminized in Red flies of both sexes compared with NonRed. We discuss alternative forms of intralocus sexual conflict that may explain these patterns.