All land plants share a deeply conserved mechanism for transcriptional responses to the auxin signaling molecules. Interactions between the components in this system - the TIR/AFB ubiquitin ligases, the Aux/IAA repressors and ARF transcription factors - are well understood, but a key question is how the dynamics of protein localization and accumulation shape the response system in vivo. We have used the minimal auxin response system in the liverwort Marchantia polymorpha to systematically map native in vivo protein accumulation using homologous recombination-mediated endogenous tagging. We found unexpected instability of the ARF proteins, which depends on targeted degradation. Through mapping the minimal region for instability, we found the MpARF degrton to be identical to that found in ARF proteins in Physcomitrium and Maize, identifying regulated proteolysis as an ancestral property of ARF proteins. ARF degradation alters stoichiometry of activating and repressing ARFs, and remodels auxin response during development. Lastly, mutating the ARF degron causes strong, auxin-insensitive phenotypes, thus identifying ARF degradation as a regulatory node in auxin response.