The 26S proteasome is best known for recognizing and degrading substrates tagged with homotypic, K48-linked polyubiquitin chains. However, emerging evidence reveals that the proteasome can also engage with more complex ubiquitin architectures. In this study, we combined single-particle cryo-electron microscopy, quantitative mass spectrometry, and chemical cross-linking to dissect the molecular basis by which the human 26S proteasome recognizes K11/K48-branched ubiquitin chains. Our structural and biochemical analyses reveal a multivalent recognition mechanism involving several subunits of the 19S regulatory particle, including RPN2, RPN8, RPN9, RPN10, and RPN11. Together, these subunits form a previously uncharacterized binding groove that specifically accommodates K11-linked ubiquitin moieties within branched chains. This structural arrangement supports the selective degradation of proteins tagged with branched ubiquitin signals. Furthermore, our data suggest that this multivalent binding pocket may be broadly adaptable to other ubiquitin chain architectures and associated regulatory factors. These findings expand our understanding of the molecular plasticity of the proteasome and underscore its central role in maintaining proteostasis through the recognition of diverse polyubiquitin signals.