The Relaxin Family Peptide Receptor 1 (RXFP1) is a unique class A GPCR with the characteristic seven transmembrane domain (TMD) in addition to a large ectodomain that consists of an N-terminal low density lipoprotein class A (LDLa) module, indispensable for receptor signalling, connected to the leucine rich repeat (LRR) domain by a 32-residue linker. The peptide hormone, relaxin, binds to the ECD and activates its receptor by a poorly understood mechanism. We recently reported that, in addition to a strong affinity binding site in the LRR domain, the linker region that tethers the N-terminal LDLa module to the LRR domain, comprises a second weak affinity-binding site, essential for activation of RXFP1 by relaxin. Upon binding to relaxin, the linker region adopts a stable helical structure orienting the LDLa module for activation. The N-terminal region of the linker may also interact with exoloop-2 of the TMD, also important for receptor activation. Our study, however, was complicated by the tendency of relaxin to dimerize at micromolar concentrations. Here we have analyzed the linker binding site using monomeric amidated relaxin and found the key residues on the linker that are involved in binding. These data also have provided insight into the formation of the activation complex that involves the binding of LDLa and linker to exoloop-2 of the TMD. Based on 1H solvent exchange rates, 1H temperature coefficients, and 15N relaxation parameters of backbone amides in the apo- and amidated relaxin-bound state of LDLa-LRR linker, the mechanism of the formation of a helical structure in the linker is reported. 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 that may also associate with the LDLa module.