Impaired social interaction is a core dimension of developmental disorders, including Fragile X Syndrome (FXS). The mouse model of FXS displays abnormal sociability and our research shows that maternal Fmr1 deficiency is sufficient to induce this phenotype. Specifically, maternal Fmr1 haploinsufficiency induces hypersociability in her wild-type (WT) male offspring, indicating developmental sensitivity to maternal FMRP levels. Oxytocin (OXT) release in the ventral tegmental area (VTA) mediates dopamine neuron activity, whose projections to the nucleus accumbens bidirectionally modulate duration of social interaction. Here we assessed whether maternal Fmr1-programmed hypersociability is associated with dysregulated OXT signaling in the VTA. Administration of intra-VTA oxytocin increased social interaction in control, but not in hypersocial maternal Fmr1-programmed mice. This effect was blocked by atosiban, an OXT receptor (OXTR) antagonist. Using a semiquantitative fISH approach, we found no differences in OXTR gene expression in VTA dopaminergic and GABAergic neurons. Immunohistochemical labeling of PVN OXT+ neurons showed no differences in OXT+ cell number, while injections of a retrograde tracer into the VTA showed comparable PVN neuron innervation of the VTA across groups. Taken together, this data shows that maternal Fmr1-dependent lack of behavioral sensitivity to intra-VTA oxytocin is not mediated by altered PVN innervation of the VTA or OXTR expression in this region. Rather, it suggests that the loss of behavioral sensitivity to oxytocin is mediated by a functional deficit in OXTRs. We therefore posit that reduced VTA sensitivity to oxytocinergic signaling may be a compensatory effect to the maternal Fmr1-dependent changes leading to the hypersocial phenotype