The evolution of eukaryotic photosynthesis marked a major transition for life on Earth, profoundly impacting the atmosphere of the Earth and evolutionary trajectory of an array of life forms. There are about ten lineages of photosynthetic eukaryotes, including Chloroplastida, Rhodophyta, and Cryptophyta. Mechanistically, eukaryotic photosynthesis arose via a symbiotic merger between a host eukaryote and either a cyanobacterial or eukaryotic photosymbiont. There are, however, many aspects of this major evolutionary transition that remain unsettled. The field, so far, has been dominated by proposals formulated following the principle of parsimony, such as the Archaeplastida hypothesis, in which a taxonomic lineage is often conceptually recognized as an individual cell (or a distinct entity). Such an assumption could lead to confusion or unrealistic interpretation of discordant genomic and phenotypic data. Here, we propose that the free-living ancestors to the plastids may have originated from a diversified lineage of cyanobacteria that were prone to symbioses, akin to some modern-day algae such as the Symbiodiniaceae dinoflagellates and Chlorella-related algae that associate with a number of unrelated host eukaryotes. This scenario, which assumes the plurality of ancestral form, better explains relatively minor but important differences that are observed in the genomes of modern-day eukaryotic algal species. Such a non-typological (or population-aware) way of thinking seems to better-model empirical data, such as discordant phylogenies between plastid and host eukaryote genes.