The sexually dimorphic extra-hypothalamic arginine-vasopressin (AVP) projections from the bed nucleus of the stria terminalis (BST) to the lateral septum (LS) and lateral habenula (LHb) are denser in males than females, and in rats require males' perinatal exposure to gonadal hormones but the absence of such exposure in females. We examined perinatal hormone effects on development of this sex difference in prairie voles (Microtus ochrogaster), which show atypical effects of hormones on sexual differentiation of some reproductive behaviors. Neonatal castration reduced the number of AVP mRNA-expressing cells in the BST and AVP immunoreactivity (IR) in the LS and LHb. Surprisingly, daily injections of 1000 µg testosterone propionate (TP) during the first postnatal week did not maintain high levels of AVP IR in neonatally-castrated males. Furthermore, perinatal treatments with TP (75, 500, or 1000 µg), testosterone (100 µg), or dihydrotestosterone (200 µg) did not masculinize AVP IR in the female LS or Lhb. In fact, 1000 µg TP reduced it in some cases. 1000 µg TP lengthened anogenital distance, though, indicating that TP was biologically active. Neonatal estrogen receptor antagonism with tamoxifen reduced AVP IR in the male LS, whereas treating neonatal females with the synthetic estrogen DES increased septal AVP IR. Tamoxifen and DES had no effects in the LHb. Similar to rats, postnatal estrogen influences some components of the extra-hypothalamic AVP system in prairie voles, but this developing system appears insensitive to exogenous androgens. Such insensitivity is atypical for a sexually dimorphic neural system in a rodent, and reflects the unusual effects of hormones on sexual differentiation of some behaviors in prairie voles.