Since the Hadean–Eoarchaean era of Earth’s history, peptides/proteins and RNA have undergone a complex evolutionary trajectory. Originating from simple monomeric units, these molecules evolved abiotically under various biochemical and biophysical constraints into functional biomolecules that contributed to the emergence of the first living cells. Within these cells, their interactions could then evolve through Darwinian selection. In this review, we examine current understanding of how protein–RNA interactions emerged under prebiotic conditions and developed into today’s iconic biomolecular machines such as the ribosome. Particular emphasis is placed on the types of physicochemical interactions accessible to early protein–RNA complexes. Special attention is given to how the limited prebiotic amino acid repertoire influenced these interactions and their roles in driving spatial organization and compartmentalization in protocellular environments.