Peptides with specific binding affinity to inorganic materials bridge biological systems with synthetic inorganic materials. Many inorganic-binding peptides were isolated using combinatorial peptide libraries without a good understanding of the interaction mechanism, which thus hinders the practical application of these peptides. Besides the amino acid composition, peptides' structure (e.g., cyclic structure constrained by disulfide bond) is believed to play an important role in their binding behavior. A cyclic peptide STB1 (-CHKKPSKSC-) was previously identified to electrostatically bind to TiO2 and SiO2, In the present study, the binding behavior (affinity and conformation) of STB1 and its linear version LSTB1 (-AHKKPSKSA-) on a TiO2 or SiO2 surface was investigated in three different contexts (i.e., free peptides, phage particles displaying peptides, and LacI-peptide fusion protein) using quartz crystal microbalance with energy dissipation measurement (QCM-D). The binding kinetics of STB1 and LSTB1 in the context of fusion protein to either metal oxide was quantitatively analyzed. LSTB1 showed similar binding behavior on both TiO2 and SiO2 surfaces. In the context of phage-displayed and LacI-hosted peptides, STB1 was found to have weaker binding affinity than LSTB1 for either metal oxide, but it was able to distinguish between SiO2 and TiO2. This is probably because LSTB1 has a much more flexible structure than STB1, as shown by the molecular dynamics simulation. The structural flexibility of LSTB1 enables it to explore a wider range of conformations to maximize its interaction with TiO2 and SiO2.