The ribosome’s common core connects all life back to a common ancestor and serves as a window to relationships among organisms. In eukaryotes, the common core contains expansion segments (ES’s) that vastly increase ribosomal RNA size. Supersized ES’s have not been observed previously in Bacteria or Archaea, and the origin of eukaryotic ES’s remains enigmatic. We discovered that the large subunit rRNA of Lokiarchaeota, the closest modern cell lineage to the last common ancestor of Archaea and Eukarya, bridges the gap in size between prokaryotic and eukaryotic rRNA. The long large subunit rRNA in Lokiarchaeota is largely due to the presence of two eukaryotic-like, supersized ES’s, ES9 and ES39, which are transcribed in situ. We applied computational models, covariation analysis, and chemical footprinting experiments to study the structure and evolution of Lokiarchaeota ES9 and ES39. We also defined the eukaryotic ES39 fold for comparison. We found that Lokiarchaeota and eukaryotic ES’s are structurally distinct: Lokiarchaeota ES39 has more and longer helices than the eukaryotic ES39 fold. Despite their structural differences, we found that Lokiarchaeota and eukaryotic ES’s originated from a common ancestor that was “primed” for evolution of larger and more complex rRNAs than those found in Bacteria and other archaea.