The class B G protein‐coupled receptor (GPCR) calcitonin receptor (CTR) is a drug target for osteoporosis and diabetes. N‐glycosylation of asparagine 130 in its extracellular domain (ECD) enhances calcitonin hormone affinity with the proximal GlcNAc residue mediating this effect through an unknown mechanism. Here, we present two crystal structures of salmon calcitonin‐bound, GlcNAc‐bearing CTR ECD and analyze the mechanism of the glycan effect. The GlcNAc does not contact the hormone. Surprisingly, the structures are nearly identical to a structure of hormone‐bound, N‐glycan‐free ECD. N‐glycosylation of CTR increased calcitonin ligand association rate and decreased its dissociation rate. Hydrogen‐deuterium exchange mass spectrometry and molecular dynamics simulations revealed that the GlcNAc stabilized an adjacent β‐sheet while increasing flexibility of the peptide‐binding site turret loop. The glycan effect extended to RAMP‐CTR amylin receptor complexes and was also conserved in the related CGRP receptor. These results reveal that N‐glycosylation can modulate GPCR function by altering receptor dynamics.Support or Funding InformationThis work was supported by NIH grant R01GM104251 to AAP, the National Research Foundation of Korea grant NRF‐2018R1A2B6001554 to KYC, and use of the crystal imaging microscope was supported by NIH COBRE award P20GM103640. DRP and JS were supported by the BBSRC grant BB/M007529/1.Graphical abstractFigure 1