Molecular interactions and mechanical properties that contribute to the stability and function of proteins are complex and of fundamental importance. In this study, we used single-molecule dynamic force spectroscopy (DFS) to explore the interactions and the unfolding energy landscape of bovine rhodopsin and bacteriorhodopsin. An analysis of the experimental data enabled the extraction of parameters that provided insights into the kinetic stability and mechanical properties of these membrane proteins. Individual structural segments of rhodopsin and bacteriorhodopsin have different properties. A core of rigid structural segments was observed in rhodopsin but not in bacteriorhodopsin. This core may reflect differences in mechanisms of protein folding between the two membrane proteins. The different structural rigidity of the two proteins may also reflect their adaptation to differing functions.