We combined traditional quantitative genetics and oligonucleotide microarrays to examine within–population genetic variation in a trait closely related to fitness. The trait, male reproductive success under competitive conditions (MCRS), is of central importance to both life-history and sexual–selection theory. We identified 27 candidate genes whose expression levels were associated with within–population variation in MCRS. ’High‚ MCRS was associated with low expression of a cytochrome P450 that causes pesticide resistance, suggesting a fitness cost to resistance. Two groups of metabolic proteins (glutathione transferases and phosphatases) were significantly over–represented, and a large portion of the candidates are genes involved in oxidative stress resistance, energy acquisition or energy storage. Genes expressed in accessory glands and testes were not over–represented among differentially expressed genes, but testis–expressed genes were significantly more likely to be upregulated in high MCRS genotypes. Finally, nine candidate genes that we identified had no previous functional annotation, and this experiment suggests that they play a role in male reproductive success.