Fe(II)-coordinating hexapeptides containing three 2,2'-bipyridine moieties as side chains were designed and synthesized. A cyclic hexapeptide having three [(2,2'-bipyridin)-5-y1]-n-alanine (D-BpaS) residues, in which D-BpaS and Gly are alternately arranged with 3-fold rotational symmetry, coordinated with Fe(II) to form a 1:1 octahedral Fe(II) peptide complex with a single facial-A configuration of the metal-centered chirality. NMR spectroscopy and molecular dynamics simulations revealed that the Fe(II) peptide complex has an apparent C-3-symmetric conformations on the NMR time scale, while the peptide backbone is subject to dynamic conformational exchange between three asymmetric beta/gamma conformations and one C-3-symmetric y/y/y conformation. The semirigid cyclic hexapeptide preferentially arranged these conformations of the small octahedral Fe(II) bipyridine complex, as well as the Ru(II) congener, to underpin the single configuration of the metal-centered chirality.