Recognizing the limitations of solid-supported lipid bilayers to reproduce the behavior of cell membranes, including bendability, transmembrane protein inclusion, and virus entry, this study describes a novel biomimetic system for cell membranes with the potential to overcome these and Other limitations. The developed strategy utilizes a hydrogel with tunable mechanical behavior that resembles those of living cells as the soft support for the phospholipid bilayer, while a polyelectrolyte multilayer film serves as an intermediate layer to facilitate the self assembly of the lipid bilayer on the soft cushion. Quartz crystal microbalance studies show that, upon coming into contact with the polyelectrolyte film, vesicles fuse and rupture to yield a robust lipid bilayer. Fluorescence recovery after photobleaching confirms the formation of a membrane, while atomic force microscopy shows a low adhesion between the indenting probe and the bilayer. More importantly, in comparison to the solid-supported lipid bilayer, the response of this biomimetic system to nanoindentation demonstrates its increased mechanical stability and bendability when assembled on a soft cushion. Hence, the developed hydrogel-supported lipid bilayers can mimic biomechanical properties of cell membranes, which will enable scientists to study and to understand biophysicochemical interactions between cell membranes and extracellular entities.