Plastidic starch synthesis in green algae and plants occurs via ADP-glucose in likeness to prokaryotes from which plastids have evolved. In contrast, floridean starch synthesis in red algae proceeds via uridine diphosphate-glucose in semblance to eukaryotic glycogen synthesis and occurs in the cytosol rather than the plastid. Given the monophyletic origin of all plastids, we investigated the origin of the enzymes of the plastid and cytosolic starch synthetic pathways to determine whether their location reflects their origin—either from the cyanobacterial endosymbiont or from the eukaryotic host. We report that, despite the compartmentalization of starch synthesis differing in green and red lineages, all but one of the enzymes of the synthetic pathways shares a common origin. Overall, the pathway of starch synthesis in both lineages represents a chimera of the host and endosymbiont glycogen synthesis pathways. Moreover, host-derived proteins function in the plastid in green algae, whereas endosymbiont-derived proteins function in the cytosol in red algae. This complexity demonstrates the impacts of integrating pathways of host with those of both primary and secondary endosymbionts during plastid evolution.