1The linkage, length, and architecture of ubiquitin (Ub) chains are all important variables 2 in providing tight control over many biological paradigms. There are clear roles for 3 branched architectures in regulating proteasome-mediated degradation, however the 4 proteins that selectively recognize and process these atypical chains are unknown. Here, 5 using synthetic and enzyme-derived ubiquitin chains along with intact mass spectrometry, 6 we report that UCH37/UCHL5, a proteasome-associated deubiquitinase, exclusively 7 cleaves K48 branched chains. The activity and selectivity toward branched chains is 8 markedly enhanced by the proteasomal Ub receptor RPN13/ADRM1. Using proteasome 9 complexes reconstituted with either active or inactive UCH37 together with protein 10 substrates modified with branched chains, we find that chain debranching promotes 11 degradation under multi-turnover conditions. These results are further supported by 12 proteome-wide pulse-chase experiments, which show that the loss of UCH37 activity 13 impairs global protein turnover. Our work therefore defines UCH37 as a debranching 14 deubiquitinase important for promoting proteasomal degradation.