Azimuthal movement of tropomyosin around the F-actin thin filament is responsible for muscle activation and relaxation. Our model of alpha-tropomyosin, derived from molecular-mechanics and electron microscopy of different contractile states, indicates that tropomyosin is rather stiff and pre-bent to present one specific face to F-actin during azimuthal transitions (Li et al., 2010, 2011). However, a new model based on cryo-EM of troponin- and myosin-free filaments proposes that the interacting-face of tropomyosin can differ significantly from that in the original model, involving a pseudo-rotation of tropomyosin about its longitudinal axis while on F-actin (von der Ecken et al., 2014). However, insufficient resolution precluded tropomyosin side-chain assignment and unambiguous interacting-face determination. We have used structural analysis and energy landscapes to examine the proposed models further. The bending of tropomyosin noted in crystal structures is, in fact, closer in direction and extent to the original model than to the new model. In addition, an interaction-map computed for tropomyosin repositioned over the F-actin surface (using the original interacting-face) shows two energy-minima - one corresponding to the “blocked-state” as in the original model, and the other related by a simple 24Å translation of tropomyosin parallel to the F-actin axis. The tropomyosin-actin complex defined by the second minimum fits seamlessly into the recent cryo-EM density, without requiring a change in interacting-face geometry (Rynkiewicz et al., 2015). We next calculated potential changes resulting from tropomyosin pseudo-rotation at multiple positions on F-actin. An analysis of interaction-energy between tropomyosin and F-actin shows that one tropomyosin interacting-face is optimized to bind actin. Together, these data suggest that movement of tropomyosin between regulatory states does not require interacting-face rotation. However, they imply that thin filament assembly may involve an interplay between initially seeded tropomyosin molecules growing from distinct binding-site regions on actin.