Sex-specific mating behaviors occur in a variety of mammals, with the medial preoptic nucleus (POM) and the ventromedial hypothalamic nucleus (VMH) mediating control of male and female sexual behavior, respectively. In birds, likewise, POM is predominantly involved in the control of male reproductive behavior, but the degree to which VMH is involved in female reproductive behavior is unclear. Here, in male and female zebra finches, a combination of aromatase immunohistochemistry and conventional tract tracing facilitated the definition of two separate but adjacent nuclei in the basal hypothalamus: an oblique band of aromatase-positive (AR+) neurons, and ventromedial to this, an ovoid, aromatase-negative (AR-) nucleus. The AR- nucleus, but not the AR+ nucleus, was here shown to receive a projection from rostral parts of the thalamic auditory nucleus ovoidalis and from the nucleus of the tractus ovoidalis. The AR- nucleus also receives an overlapping, major projection from previously uncharted regions of the medial arcopallium and a minor projection from the caudomedial nidopallium. Both the AR- and the AR+ nuclei project to the intercollicular nucleus of the midbrain. No obvious sex differences in either the pattern of AR immunoreactivity or of the afferent projections to the AR- nucleus were observed. The significance of these results in terms of the acoustic control of avian reproductive behavior is discussed, and a comparison with the organization of VMH afferents in lizards suggests a homologous similarity of the caudal telencephalon in sauropsids.