The main objective is to offer a functionally coherent counter-narrative to the polarized views prevailing now about the complex ‘Eukaryogenesis problem’ versus the “primitive” nature ascribed to so-called “Prokaryotes” (termed Akaryotes herein). The paradigm shift presented aims at bridging the conceptual gap between the rudimentary beginnings of biomolecular cooperativity on a pristine Earth (the Origins of Life or OoL) and the beginnings of lineage-wise diversification toward Darwinean speciation in the Tree of Life (or ToL). Although the research field as a whole is not aware of a corresponding ‘Prokaryogenesis problem’, the evolutionary process resulting in the partly independent archaeal and bacterial cell types is not fully understood. The present paper provides an explanation for these problems based on coevolutionary complementarity at multiple levels. The unconventional model connects various stages from “neighborhood selection” in film-like layers of unbounded “surface protoplasm” based on short “statistical proteins”, via a closely knit “peptide/RNA partnership” in the “making of genes”, toward the “making of genomes” in several RNA-to-DNA transitions. Three virus-related plasmids carrying different DNA replicases may have initiated the vertical stability of hereditable lineages that led to the three “domains” of organismal life, with a fourth lineage ending in eukaryotic organelles. These partly independent transitions established DNA as a late-comer of fundamental biomolecules.