Stress is a well-known cause of reproductive dysfunction in many species, including birds, rodents, and humans. However, little is known of the genomic basis for this dysfunction and how it may differ between the sexes. Using the classic reproductive model of the rock dove (Columba livia), we conducted the most in-depth investigation to date of how stress affects all gene transcription of a biological system essential for facilitating reproduction - the hypothalamic-pituitary-gonadal (HPG) axis. The HPG transcriptome responded to stress in both sexes, but females exhibited more differential expression than males, and these stress responsive genes were mostly unique to females. This result may be due to 1) fluctuations in the female endocrine environment to facilitate ovulation and follicle maturation, and 2) their evolutionary history. We offer a vital genomic foundation on which sex-specific reproductive dysfunction can be studied, as well as novel gene targets for genetic intervention and therapy investigations.