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.