Free-living male song sparrows experience three annually repeating life history stages associated with differential expression of sex steroid-dependent reproductive and aggressive behavior. In the breeding stage, they display reproductive and aggressive behavior and have elevated circulating testosterone levels. During molt, males show little or no aggression and no reproductive behavior, and have basal levels of circulating testosterone. In the non-breeding stage, they display high levels of aggression and no reproductive behavior, and have basal levels of circulating testosterone. In order to understand more fully the neural regulation of seasonal aggressive and reproductive behavior, birds were collected during all three life history stages, and levels of neural aromatase, androgen receptor (AR), and estrogen receptor α (ERα) and β (ERβ) mRNA expression were measured. Breeding males had the highest levels of aromatase expression in both the preoptic area (POA) and medial preoptic area/medial bed nucleus of the stria terminalis (mPOA/BSTm), and the highest AR expression levels in the POA, consistent with the well-established role these regions play in the regulation of male reproductive behavior. Aromatase expression in the ventromedial nucleus of the hypothalamus (VMH) was higher during breeding and non-breeding compared with molt, suggesting that the VMH may play a role in the estrogen-dependent regulation of aggression in this species. AR expression also varied in medial HVC and pvMSt, a newly described periventricular region in the medial striatum. ERα and ERβ mRNA expression did not vary seasonally in any brain region examined, suggesting that estrogen-dependent changes in behavior are mediated by differences in neural estrogen synthesis. J. Comp. Neurol. 518:3819–3835, 2010. © 2010 Wiley-Liss, Inc.