Cellular membranes are natural nanoengineering devices, where matter transport, information processing, and energy conversion across the nanoscale boundaries are mediated by membrane proteins (MPs). Despite the great potential of MPs for nanotechnologies, their broad utility in engineered systems is limited by the fluidic and often labile nature of MP-supporting membranes. Little is known on how to direct spontaneous reconstitution of MPs into robust synthetic nanomembranes or how to tune MP functions through rational design of these membranes. Here we report that proteorhodopsin (PR), a light-driven proton pump, can be spontaneously reconstituted into "frozen" (i.e., glassy state) amphiphilic block copolymer membranes via a charge-interaction-directed reconstitution mechanism. We show that PR is not enslaved by a fluidic or lipid-based membrane environment. Rather, well-defined block copolymer nanomembranes, with their tunable membrane moduli, act as allosteric regulators to support the structural integrity and function of PR. Versatile membrane designs exist to modulate the conformational energetics of reconstituted MPs, therefore optimizing proteomembrane stability and performance in synthetic systems.