Because fossils from the time when cellular life originated and diversified are scant and difficult to interpret1, alternative means to investigate the ecology of the Last Universal Common Ancestor (LUCA) and of the ancestors of the three domains of life are of great scientific value. It was recently recognized that footprints of the effect of temperature on ancestral organisms could be uncovered in extant genomes2–4. Accordingly, analyses of resurrected proteins predicted that the bacterial ancestor was thermophilic and that Bacteria subsequently adapted to lower temperatures3,4. Since the archaeal ancestor is also thought to have been thermophilic5, LUCA was parsimoniously inferred as thermophilic too. However, an analysis of ribosomal RNAs supported the hypothesis of a non-hyperthermophilic LUCA2. Here we show that both rRNA and protein sequences analysed with advanced, realistic models of molecular evolution6,7 provide independent support for two phases in the history of environmental temperature changes over the tree of life: in the first period, thermotolerance increased from a mesophilic LUCA to thermophilic ancestors of Bacteria and of Archaea-Eukaryota; in the second period, it decreased. Therefore, the two lineages descending from LUCA and leading to the ancestors of Bacteria and Archaea-Eukaryota convergently adapted to high temperatures, maybe in response to a climate change of the early Earth1,8,9, and/or aided by the transition from an RNA genome in LUCA to organisms with more thermostable DNA genomes10,11. This analysis unifies apparently contradictory results2–4 into a coherent depiction of the evolution of an ecological trait over the entire tree of life.