Life in its molecular context is characterized by the challenge of orchestrating structure, energy and information processes through compartmentalization and chemical transformations amenable to mimicry of protocell models. Here we present an alternative protocell model incorporating dynamic membranes based on amphiphilic elastin‐like proteins (ELPs) rather than phospholipids. For the first time we demonstrate the feasibility of combining vesicular membrane formation and biocatalytic activity with molecular entities of a single class: proteins. The presented self‐assembled protein‐membrane‐based compartments (PMBCs) accommodate either an anabolic reaction, based on free DNA ligase as an example of information transformation processes, or a catabolic process. We present a catabolic process based on a single molecular entity combining an amphiphilic protein with tobacco etch virus (TEV) protease as part of the enclosure of a reaction space and facilitating selective catalytic transformations. Combining compartmentalization and biocatalytic activity by utilizing an amphiphilic molecular building block with and without enzyme functionalization enables new strategies in bottom‐up synthetic biology, regenerative medicine, pharmaceutical science and biotechnology. A generalizable molecular platform for minimalist cell design: Essential features of extant cells include compartmentalization and biocatalytic activity. In this context we designed a minimal cell system in which the protocellular membrane was made up solely of protein components, by use of amphiphilic block‐domain elastin‐like proteins together with free or conjugated enzymes.