Male and female reproductive behaviors in Drosophila melanogaster are vastly different, but the neurons that express sex-specifically spliced fruitless transcripts (fru P1) underlie these behaviors in both sexes. How a similar set of neurons can drive such different behaviors is an unresolved question in neurogenetics. A particular challenge is that fru P1-expressing neurons comprise only 2-5% of the adult nervous system, and so inferences made in studies of adult head tissue or even the whole brain are limited. To assess gene expression in the fru P1- expressing cells we used Translating Ribosome Affinity Purification (TRAP). This technique allows us to conduct a sensitive, cell-specific assay of gene expression by identifying the actively translated pool of mRNAs from fru P1-expressing neurons. Additionally, to examine the changes in gene expression across development we assay three different time-points in the fly life cycle—48hr pupae, 0-24hr adult, and 10 day adults. Here, we present results on the 0-24hr adults and find that the male and female fru P1-expressing neurons have a shared set of 7,967 genes identified by TRAP that form a distinct repertoire relative to those identified from TRAP analyses of all neurons in the adult head. Further, there are genes that have sex-biased TRAP abundance in fru P1-expressing neurons, with the majority of these genes having male-biased TRAP abundance. This suggests an underlying mechanism to generate dimorphism in behavior, with a transcript repertoire that specifies male and female behaviors present in both sexes and a large additional set of genes with expression in the male. Thus, these additional genes could invoke the male-specific behaviors by establishing cell fate in a similar context of gene expression observed in females. These results suggest a possible global mechanism for how distinct behaviors can arise in different environments from a shared set of neurons.