Abstract: Cofilin/ADF proteins play key roles in the dynamics of actin. We used cryo-electron microscopy of uniformly decorated actin-cofilin filaments to show that the cofilin induced change in the filament twist is due to a unique conformation of the actin molecule unrelated to any previously observed state. The changes between the actin protomer in naked F-actin and in the actin-cofilin filament are greater than the conformational changes between G- and F-actin. Cofilin/ADF proteins efficiently depolymerize F-actin only when bound at low stoichiometry to actin filaments. We also used cryo electron microscopy to reveal the structure of F-actin decorated with sub-stoichiometric amounts of cofilin. Our results suggest that the structural state of actin protomers found within the uniformly decorated actin-cofilin filaments can propagate towards the naked regions, and this cooperative propagation is uncoupled from the change in the helical twist of F-actin upon interaction with cofilin. This illustrates the structural plasticity of actin and provides a structural mechanism for actin depolymerization by the ADF/cofilin proteins.