We present large subunit (LSU) and internal transcribed spacer (ITS) rDNA based phylogenies of symbiotic dinoflagellates retrieved from single-cell planktonic foraminifera collected around the world. All modern foraminiferal species involved in such symbiosis are included in our analyses. The pelagic symbiotic dinoflagellates form a monophyletic group sister to the Symbiodinium species complex found in coastal-benthic environments. The pelagic symbionts are descendants of free-living species and, together with the coastal-benthic Symbiodinium spp., they originated from the early Mesozoic suessiacean family represented by the extant Polarella glacialis. Out of hundreds of single planktonic foraminifera examined, 21 unique pelagic symbiont ribotypes were recognized, which could be divided into 2 main clades and 4 genetic subgroups, We observed an absence of specificity between the symbiont genetic types and the host genetic and morphological species. A few foraminifera even harbored dinoflagellates of more than one genetic subgroup. This genetic flexibility may be constrained by the fast life cycles of pelagic single-cell hosts, which acquire symbionts de novo from the ambient water at each generation. The obligatory transitional free-living stage of pelagic symbionts prior to acquisition by foraminiferal hosts may also explain their significantly lower rates of DNA substitution in comparison to their coastal-benthic relatives. We propose that the open ocean ecosystem has maintained photosymbioses involving a relatively low genetic diversity, but an extreme flexibility in the relationships between both partners, which also preserved their ancestral ability for independent life.