AMPK and TOR protein kinases are the major control points of energy signalling in eukaryotic cells and organisms. They form the core of a complex regulatory network to coordinate metabolic activities in the cytosol with those in mitochondria and plastids. Despite its relevance, it is still unclear when and how this regulatory pathway was formed during evolution, and to what extent its representations in the major eukaryotic lineages resemble each other. Here we have traced 153 essential proteins forming the human AMPK-TOR pathways across 413 species representing all three domains of life, and subsequently through time. Further, we have characterized these traced proteins based on their feature architecture similarities to obtain a functionally meaningful interpretation of the phylogenetic profiles. The resulting phylogenetic profiles indicate the presence of primordial core pathways including 7 proto-kinases in the last eukaryotic common ancestor. The evolutionary roots of the oldest components of the AMPK pathway, however, extend into the pre-eukaryotic era, and descendants of these ancient proteins can still be found in contemporary prokaryotes. The TOR complex in turn appears as a eukaryotic invention, possibly to aid in retrograde signalling between the mitochondria and the remainder of the cell. Within the eukaryotes, the two pathways display beyond the conserved cores, a considerable plasticity. Most notably, KING1, the protein originally assigned as the gamma subunit of AMPK in plants, is more closely related to the yeast SDS23 gene family then to the gamma subunits in animals or fungi. This suggests that also its functionality differs from that of a canonical AMPK gamma subunit.