jats:titleAbstract</jats:title>jats:pChlorophyll‐based photosynthesis has fuelled the biosphere since at least the early <jats:styled-content style="fixed-case">A</jats:styled-content>rchean, but it was the ecological takeover of oxygenic cyanobacteria in the early <jats:styled-content style="fixed-case">P</jats:styled-content>alaeoproterozoic, and of photosynthetic eukaryotes in the late <jats:styled-content style="fixed-case">N</jats:styled-content>eoproterozoic, that gave rise to a recognizably modern ocean–atmosphere system. The fossil record offers a unique view of photosynthesis in deep time, but is deeply compromised by differential preservation and non‐diagnostic morphologies. The pervasively polyphyletic expression of modern cyanobacterial phenotypes means that few <jats:styled-content style="fixed-case">P</jats:styled-content>roterozoic fossils are likely to be members of extant clades; rather than billion‐year stasis, their similarity to modern counterparts is better interpreted as a combination of serial convergence and extinction, facilitated by high levels of horizontal gene transfer. There are few grounds for identifying cyanobacterial akinetes or crown‐group <jats:styled-content style="fixed-case">N</jats:styled-content>ostocales in the <jats:styled-content style="fixed-case">P</jats:styled-content>roterozoic record. Such recognition undermines the results of various ancestral state reconstruction analyses, as well as molecular clock estimates calibrated against demonstrably problematic <jats:styled-content style="fixed-case">P</jats:styled-content>roterozoic fossils. Eukaryotic organisms are likely to have acquired their (stem‐group nostocalean) photoendosymbionts/plastids by at least the <jats:styled-content style="fixed-case">P</jats:styled-content>alaeoproterozoic, but remained ecologically marginalized by incumbent cyanobacteria until the late <jats:styled-content style="fixed-case">N</jats:styled-content>eoproterozoic appearance of suspension‐feeding animals.</jats:p>