The eukaryotic organelles mitochondrion and plastid originated from eubacterial endosymbionts. Here we propose that, in both cases, prokaryote-to-organelle conversion was driven by the internalization of host-encoded factors progressing from the outer membrane of the endosymbionts towards the intermembrane space, inner membrane and finally the organelle interior. This was made possible by an outside-to-inside establishment in the endosymbionts of host-controlled protein-sorting components, which enabled the gradual integration of organelle functions into the nuclear genome. Such a convergent trajectory for mitochondrion and plastid establishment suggests a novel paradigm for organelle evolution that affects theories of eukaryogenesis.