Aggression in territorial social systems is easy to interpret because the benefits of territorial defence mostly accrue to the territorial holder. However, in non-territorial systems, high aggression seems puzzling and raises intriguing evolutionary questions. We describe extreme rates of despotism between age classes in a passerine bird, the painted bunting (
Passerina ciris
), during the pre-moulting period. Aggressive encounters were not associated with aggressors gaining immediate access to resources. Instead, conspecifics, and even other species, were pursued as though being harassed; this aggression generated an ideal despotic habitat distribution such that densities of adult males were higher in high-quality sites. Aggression was not a by-product of elevated testosterone carried over from the breeding season but, rather, appeared associated with dehydroepiandrosterone, a hormone that changes rates of aggression in non-breeding birds without generating the detrimental effects of high testosterone titres that control aggression in the breeding season. This extraordinary pre-moult aggression seems puzzling because individual buntings do not hold defined territories during their moult. We speculate that this high aggression evolved as a means of regulating the number of conspecifics that moulted in what were historically small habitat patches with limited food for supporting the extremely rapid moults of painted buntings.