AbstractTitin is a giant protein that provides elasticity to muscle. As the sarcomere is stretched, titin extends hierarchically according to the mechanics of its segments. Whether titin's globular domains unfold during this process and how such unfolded domains might contribute to muscle contractility are strongly debated. To explore the force‐dependent folding mechanisms, here we manipulated skeletal‐muscle titin molecules with high‐resolution optical tweezers. In force‐clamp mode, after quenching the force (<10 pN), extension fluctuated without resolvable discrete events. In position‐clamp experiments, the time‐dependent force trace contained rapid fluctuations and a gradual increase of average force, indicating that titin can develop force via dynamic transitions between its structural states en route to the native conformation. In 4 M urea, which destabilizes H‐bonds hence the consolidated native domain structure, the net force increase disappeared but the fluctuations persisted. Thus, whereas net force generation is caused by the ensemble folding of the elastically‐coupled domains, force fluctuations arise due to a dynamic equilibrium between unfolded and molten‐globule states. Monte–Carlo simulations incorporating a compact molten‐globule intermediate in the folding landscape recovered all features of our nanomechanics results. The ensemble molten‐globule dynamics delivers significant added contractility that may assist sarcomere mechanics, and it may reduce the dissipative energy loss associated with titin unfolding/refolding during muscle contraction/relaxation cycles.