The peptide hormone INSL3 and its receptor RXFP2 have co-evolved alongside relaxin and its receptor RXFP1. Both RXFP1 and RXFP2 are G protein-coupled receptors (GPCRs) containing the hallmark seven transmembrane (TM) helices in addition to a distinct ecto-domain of Leucine-rich repeats (LRRs) and a single Low Density Lipoprotein Class-A (LDLa) module at the N-terminus. RXFP1 and RXFP2 are the only mammalian GPCRs described as containing an LDLa, and its removal does not perturb primary ligand binding to the LRRs, however signaling is abolished. This presents a general mechanism whereby ligand binding induces a conformational change of the receptor to position the LDLa to elicit a signal response. Although the LDLa interaction site has not been identified the residues important to the action have been mapped within RXFP1 LDLa. In this study we comprehensively study the RXFP2 LDLa module. We solve its structure using Nuclear Magnetic Resonance and concurrently investigate the signaling of an RXFP2 with the LDLa removed (RXFP2-short), confirming that the LDLa is essential to signaling. We then replaced the LDLa with the second ligand-binding module from the LDL receptor, LB2, creating RXFP2-LB2. Unlike the equivalent RXFP1-LB2 chimera, signaling is rescued albeit modestly. Guided by the NMR structure we dissected regions of the RXFP2 LDLa to identify specific residues that are important to signal activation. We determine that although the module is important to the activation of RXFP2, unlike the RXFP1 receptor, specific residues in the N-terminus of the domain are not involved in signal activation.