Auxin response critically depends on the concentrations and stoichiometry of competing A- and B-class AUXIN RESPONSE FACTOR (ARF) proteins. In Marchantia polymorpha, both A- and B-ARFs are unstable, and here we identify a minimal necessary and sufficient region for ARF degradation that is critical for development, and auxin response. Through comparative analysis, we find that ARF instability likely preceded the emergence of the auxin response system.