In songbirds, song learning and production are regulated by the song control system. How the rest of the brain interacts with song nuclei to ensure that song is produced in an appropriate context is not yet clear. In male European starlings (Sturnus vulgaris), breeding context song is sexually motivated whereas non-breeding context song is more broadly socially motivated. Brain regions involved in regulating social behavior might differentially regulate starling song depending upon the context in which it is produced. Here, we compared the number of ZENK-labeled cells in song and social behavior nuclei in starlings singing in either a breeding or a non-breeding context. Numbers of ZENK-labeled cells in HVC related positively to song produced in both contexts. Interestingly, numbers of ZENK-labeled cells in one subdivision of the lateral septum (LS) related negatively to breeding context song but positively to non-breeding context song. In a subdivision of the medial bed nucleus of the stria terminalis (BSTm) ZENK labeling only related positively to non-breeding context song whereas in the ventromedial nucleus of the hypothalamus (VMH) ZENK labeling showed a tighter positive relationship with breeding context song. Together, these findings indicate that social behavior brain regions outside of the song control system regulate singing behavior differently depending upon whether song is sexually or more broadly socially motivated. Breeding context-dependent regulation of song by LS, BSTm, and VMH suggests that these nuclei may be central to adjusting song production so that it occurs in response to appropriate social and environmental stimuli. Keywords songbird; season; social context; ZENK; high vocal center; lateral septum; bed nucleus of the stria terminalis; ventromedial nucleus of hypothalamus