The retrosplenial cortex (RSC) is known for its pivotal role in contextual fear conditioning, receiving inputs from both corticocortical and subcortical pathways, including the nucleus incertus in the pontine tegmentum. This region contains a GABAergic projection rich in relaxin-3 (RLN3), which acts via its Gi/o-protein-coupled receptor, RXFP3. To investigate the involvement of this peptidergic system in contextual fear conditioning, we bilaterally injected adult rat RSC with an adeno-associated virus (AAV) expressing the chimeric RXFP3 agonist R3/I5 or a control AAV and subjected them to contextual fear conditioning. Rats injected with R3/I5 did not exhibit differences during conditioning but showed a significantly delayed extinction phase compared to control-injected and naïve rats. Additionally, we administered acute bilateral injections of the specific RXFP3 agonist peptide, RXFP3-Analogue 2 (A2), into the RSC. While A2 treatment before each extinction trial did not affect the process, administration before each acquisition trial led to a delayed extinction. Anatomical studies revealed an enrichment of RLN3-immunoreactive nerve fibers in deep layers of the RSC, with a higher co-localization of RXFP3 mRNA with vesicular GABA transporter (vGAT) mRNA than with vesicular glutamate transporter-1 (vGLUT1) mRNA, indicating the involvement of RLN3/RXFP3 signaling in intrinsic inhibitory circuits within the RSC. These findings suggest that contextual conditioning in the RSC involves RLN3-mediated activation of local inhibitory neurons, resulting in enhanced memory acquisition and subsequently delaying the extinction process.