Supported poly(ethylene glycol)-lipid bilayers (PEG-SLBs) are of interest as scaffolds in future generations of transmembrane protein sensor platforms and in their own right as model systems to investigate the behavior of glycosylated biological membranes. We investigate the effect of PEG-lipid concentration from the PEG dilute mushroom to brush regime in PEG-SLBs on lipid mobility and membrane behavior under locally applied compression force. Fluorescence recovery after photobleaching (FRAP) measurements demonstrated a gradual transition of the POPC lipid bilayer from liquid crystalline to gel phase for a PEG-lipid concentration below 10 mol% and PEG molecular weight of 2000 Da. The observed control of lipid phase behavior already at low interacting polymer lipid concentrations could have wider implications for the understanding of biological membrane systems. Further mechanical properties of the PEG-SLBs were probed by force–distance measurements with an atomic force microscope (AFM). Significant differences in the compression of mobile and immobile tethered polymer chains were observed. The results were interpreted through a model describing compression force profiles for polymers attached to mobile tethers, which reproduces a unique transition observed as mobile polymer tethers are locally depleted under compression.