A balance between protein synthesis and degradation is necessary to maintain cellular homeostasis. Failure to triage aberrant proteins may result in their accumulation and aggregation in the cytosol. The VCP-BAG6 complex facilitates a wide variety of ubiquitin-mediated quality control events at the ER; both prior to ER translocation as well as during ER associated degradation (ERAD). Yet, how ubiquitylated clients associated with BAG6 are recognized by VCP for proteasomal degradation is presently unknown. We have identified UBXN1 as the VCP adaptor in BAG6-dependent processes occurring prior to ER insertion but not during ERAD. Loss of VCP-UBXN1 results in the inappropriate stabilization of ubiquitylated BAG6 clients; their accumulation in insoluble aggregates and sensitizes cells to proteotoxic stress. Our results identify how VCP is specifically targeted to ubiquitylated substrates in the BAG6 triage pathway and suggest that degradation of ubiquitylated clients by the proteasome is reliant on UBXN1 association with ubiquitylated substrates and VCP catalytic activity.