Hybrid vesicles consisting of natural phospholipids and synthetic amphiphilic copoly- mers have shown remarkable material properties and potential for biotechnology, com- bining the robustness of polymers with the biocompatibility of phospholipid mem- branes. To predict and optimize the mixing behavior of lipids and copolymers, as well as understand the interaction between the hybrid membrane and macromolecules like membrane proteins, a comprehensive understanding at the molecular level is essen- tial. This can be achieved by a combination of molecular dynamics simulations and experiments. Here, simulations of POPC and PBd22-b-PEO14 hybrid membranes are shown, uncovering different copolymer configurations depending on the polymer-to- lipid ratio. High polymer concentrations created thicker membranes with an extended polymer conformation, while high lipid content led to the collapse of the polymer chain. High concentration of polymer further correlated with a decreased area com- pression modulus and altered lateral pressure profiles, hypothesized to result in the experimentally-observed improvement in membrane protein reconstitution and resis- tance towards destabilization by detergents. Finally, simulations of a WALP peptide embedded in the bilayer showed that only membranes with up to 50% polymer con- tent favored a transmembrane configuration. These simulations correlate with previous and new experimental results and provide a deeper understanding of the properties of lipid-copolymer hybrid membranes.