Oxytocin (OT) and vasopressin (VP) are considered to be principal neurochemical substrates of bonding in monogamous species. We have reported previously that conditioning of a sexual partner preference in male rats resulted in conditioned activation of OT and VP neurons in hypothalamic paraventricular and supraoptc nuclei. Here we asked whether such conditioning would also alter OT or VP receptor densities. Sexually naïve male rats were assigned to one of three groups (n = 15/group). The Paired group received 9 copulatory training trials with sexually receptive females scented with a neutral almond odor. The Unpaired group received 9 copulatory training trials with unscented sexually receptive females. The Naïve group were not given sexual experience. Paired and Unpaired males were given a final test in an open field with two receptive females, one scented and the other unscented, to assess the development of conditioned ejaculatory preference (CEP), which was expressed significantly in the Paired group. Brains from rats in the three groups were then assessed for OT receptor (OTR) or VP1a receptor (VPR) densities within cortical, limbic and hypothalamic structures using autoradiography with selective 125I-labeled receptor ligands. Sexual experience alone increased OTR significantly in the medial preoptic area (mPOA), ventromedial hypothalamus (VMH), and central nucleus of the amygdala (CeA) in both Paired- and Unpaired-trained males compared to sexually Naïve males. No differences were found for experience on VPR densities in any region. These data add to a growing body of evidence that sexual experience alters brain function and processing of sex-related cues, and suggest that enhanced activation of OTRs in the mPOA, VMH, and CeA by conditioned OT release in those regions may underlie CEP in the male rat.