The song control system is a group of discrete interconnected nuclei found in the brains of all songbirds (suborder Passeri). Previous studies have reported a positive relationship between sex differences in song nucleus volumes and sex differences in song behavior across numerous songbird species, with species exhibiting greater sex differences in behavior also exhibiting greater sex differences in the brain. This body of comparative research, however, has failed to incorporate data from a bird species in which females sing more than males. In this study, we examine song nucleus volumes in both sexes of the streak-backed oriole (Icterus pustulatus), a New World blackbird with a female bias in song rate and similar song complexity between the sexes. Results from this neuroanatomical analysis are contrary to what was to be expected from previous research: despite the female bias in song rate, males have a significantly larger HVC and area X song nucleus volumes. Specifically, male HVC was 75% larger than that of females, and male area X was 64% larger than that of females. There was no significant sex difference in the size of the nucleus robustus arcopallialis. The lack of a positive relationship between song nuclei and singing behavior in these orioles demonstrates that our current understanding of song modulation via the song control system may be overly reliant on basic measures such as total volumes.