Phase separation, and coacervates in particular, may have played a key role in the transition from an abiotic to a biotic world, in providing early membrane‐less compartments and promoting metabolism. Herein, we highlight another potential role of coacervates in providing the milieu in which short abiotically formed peptides evolved gradually into structured, functional proteins. Coacervates, amyloids, and other rudimentary forms of self‐assembly enable short peptides to form supramolecular structures, thus providing the level of structural pre‐organization and complexity needed for biochemical function. Coacervates, however, are unique in also enabling co‐assembly of peptides and nucleic acids, and in promoting the acquisition of helical structures. These two properties, combined with their potential to promote the synthesis of biopolymers, make coacervates a feasible springboard for the emergence of the early nucleic acids binding proteins. Herein, we outline this putative evolutionary scenario and the evidence supporting it, also regarding the emergence of cationic amino acids that are critical to coacervate formation.