Natural elastomeric fibres play central structural and functional roles in a variety of tissues produced by many organisms from diverse Phyla. Most of these fibres feature amorphous structure and their long-range elastic response is well described within the framework of entropic (rubber-like) elasticity. Recently, it has been recognized that long-range reversible deformation can also occur in biomacromolecular fibres or networks that feature significant secondary structure and long-range order. Their elastomeric response is then associated with conformational changes of the backbone of the constitutive protein-based polymers. Under axially imposed loads, several groups of proteins whose structure is dominated by α-helical coiled-coil structures can undergo unfolding transitions and secondary structure transformations, for example from coiled-coil α-helices to β-sheet strands. In contrast to rubber-like biopolymers, the retractive elastic force in these biomacromolecular materials is not dominated by a return to a maximum entropic state, but is mostly the result of variations in internal energy associated with the conformational changes. Here, a review of α-helix based elastomeric materials is presented that encompasses examples and experimental evidence across multiple length scales, from the molecular to the macroscopic scale. We begin by summarizing the basic thermodynamic formalism of thermoelasticity. While this formalism is well established for amorphous (entropically-dominated) fibres under tensile loading, its extension towards conformational (internal energy-dominated) elasticity is less known. Recent experimental evidence as well as corroborating computer simulations are then reviewed and discussed in the light of secondary structure and nano-scale features of these biopolymers. Comparisons are also drawn with physiologically important structural fibres that share common characteristics at the molecular and the nano-scale, including intermediate filament (IF) proteins from the cell cytoskeleton, myosins from motor proteins, and fibrin from blood clot. We conclude with a discussion on future directions and opportunities for these materials from a biomimetics engineering perspective.