In a well-studied model of social behaviour, male zebra finches sing directed song to court females and undirected song, used possibly for practice or advertisement. Although the two song types are similar, the level of neural activity and expression of the immediate early gene egr-1 are higher during undirected than during directed singing in the lateral part of the basal ganglia song nucleus AreaX (LAreaX) and its efferent pallial song nuclei lateral magnocellular nucleus of the anterior nidopallium (LMAN) and the robust nucleus of the arcopallium (RA). As social interactions are dependent on brain motivation systems, here we test the hypothesis that the midbrain ventral tegmental area-substantia nigra pars compacta (VTA-SNc) complex, which provides a strong dopaminergic input to LAreaX, is a source of this modulation. Using egr-1 expression, we show that GABAergic interneurons in VTA-SNc are more active during directed courtship singing than during undirected singing. We also found that unilateral removal of VTA-SNc input reduced singing-dependent gene expression in ipsilateral LAreaX during both social contexts but it did not eliminate social context differences in LAreaX. In contrast, such lesions reduced and eliminated the social context differences in efferent nuclei LMAN and RA, respectively. These results suggest that VTA-SNc is not solely responsible for the social context gene regulation in LAreaX, but that VTA-SNc input to LAreaX enhances the singing-regulated gene expression in this nucleus and, either through LAreaX or through direct projections to LMAN and RA, VTA-SNc is necessary for context-dependent gene regulation in these efferent nuclei.