The folding and function of proteins is guided by their multidimensional energy landscapes. Local corrugations on rugged energy surfaces determine the dynamics of functionally related conformational changes and molecular flexibilities. By varying the temperature during the force-induced unfolding of the membrane protein bacteriorhodopsin, we directly determined the energy roughness of individual transmembrane α-helices. All helices have rugged energy surfaces with an overall roughness scale of 4-6 kBT, in line with the vital roles of transmembrane helices as functional and structural building blocks. Interestingly, the mechanical unfolding of misfolded membrane proteins in vivo is likely to occur on similarly energy rugged surfaces, which may also provide an energetic framework for small vertical motions of functionally relevant helices. Finally, our results also indicate that transmembrane protein structures can have rough energy surfaces despite their highly restricted conformational spaces in confining lipid bilayer environments.