The ectodomain of the relaxin GPCR receptor, RXFP1, comprises an N-terminal LDLa module, essential for activation, tethered to a leucine-rich repeat (LRR) domain by a 32-residue linker. Activation is proposed to proceed by relaxin binding with strong affinity to the LRR domain and then, through an unknown process, enable the LDLa module, proposed to be a tethered agonist, to bind and activate the transmembrane domain. As the linker shows poor sequence identity amongst homologues, it has been thought of as simply a disordered region to tether the LDLa module to the receptor. We have found mutations within a conserved region of the linker immediately C-terminal to the LDLa module (GDNNGW, residues 41-46) significantly weakens relaxin affinity, suggesting an additional binding site. Using NMR spectroscopy and titrations of 15N-labelled LDLa-linker with relaxin or a paramagnetic (Mn2+) labelled relaxin, we have elucidated a discrete relaxin-binding site (residues 46-63) on the linker. Additional NMR experiments show residues 49-52 of the linker have a weak propensity for helix, which on relaxin titration stabilizes (Sethi A et al., Nat Comm, 2016). While a lack of 1H-1H NOEs suggest that the linker extends away from the LDLa module, characterization of 15N-relaxation parameters in the absence and presence of relaxin suggests that the linker weakly associates with the LDLa module. We hypothesize that LDLa-LRR linker and relaxin binding is a two-step mechanism in which partially ordered conformations of the linker form a complex with relaxin and then rapidly rearrange to form a stable helical structure, suggesting that the role of the LDLa module, along with relaxin, is to stabilize a helical conformation of the linker, especially the residues GDNNGW, which then serves as the true agonist for its receptor activation.