Dehydroepiandrosterone ( DHEA) is a testosterone/oestrogen precursor and known modulator of vertebrate aggression. Male song sparrows ( Melospiza melodia morphna) show high aggression during breeding and nonbreeding life‐history stages when circulating DHEA levels are high, and low aggression during molt when DHEA levels are low. We previously showed that androgen receptor and aromatase mRNA expression are higher during breeding and/or nonbreeding in brain regions associated with reproductive and aggressive behaviour, although the potential role of DHEA in mediating these seasonal changes remained unclear. In the present study, nonbreeding male song sparrows were captured and held in the laboratory under short days (8 : 16 h light/dark cycle) and implanted with s.c. DHEA‐filled or empty (control) implants for 14 days. DHEA implants increased aggression in a laboratory‐based simulated territorial intrusion. Brains of DHEA‐implanted birds showed higher aromatase mRNA expression in the preoptic area ( POA) and higher androgen receptor mRNA expression in the periventricular nucleus of the medial striatum (pv MSt) and ventromedial nucleus of the hypothalamus. The DHEA‐induced increases in aromatase expression in the POA and androgen receptor expression in the pv MSt are consistent with previously reported seasonal increases in these markers associated with naturally elevated DHEA levels. This suggests that DHEA facilitates seasonal increases in aggression in nonbreeding male song sparrows by up‐regulating steroid signalling/synthesis machinery in a brain region‐specific fashion.