There are nearly 100 DUBs encoded by the human genome, but only three of which are currently considered to be proteasome-associated, here named as – pDUBs: Rpn11/PSMD14, Ubp6/USP14 and UCH37/UCHL5. Only Rpn11 is an integral subunit of the proteasome, whereas the other two dock transiently and peripherally at dedicated proteasomal subunits. UCHL5 binds to Rpn13 and has been ascribed to prune branched K48 Ub chains from the substrate. USP14 reportedly binds to the proteasome via Rpn1 through its Ubl-domain and acts as a gatekeeper during protein degradation by trimming supernumerary K48 ubiquitin modifications on substrates. Proteasome function is often modulated by transiently associated proteins, including these pDUBs, many of which bear ubiquitin-like (Ubl) domains. In addition to USP14, around ~20 human DUBs have Ubl-domains, but their propensities for proteasome interaction are not well-established. In this line of hypothesis that there could be additional pDUBS, we obtained evidence of yet another DUB that associates with human 26S proteasomes through its Ubl-domain but without competing with other pDUB associations. By characterizing and establishing its proteasome interaction both in vitro and in vivo we conclude that it is the fourth pDUB after Rpn11, Uchl5, and Usp14. Interestingly, this pDUB alters the manner by which the proteasome processes ubiquitin-conjugated conjugated and facilitates substrate selection. Further understanding of its substrate specificity on the proteasome and the timing of engagement in a cellular context would be fundamental to understanding its overall contribution towards proteasome function.