The extracellular aggregation of proteins into proteotoxic oligomers and amyloid fibrils is implicated in the onset and pathology of numerous diseases referred to as amyloid diseases. All of the proteins that aggregate extracellularly in association with amyloid disease pathogenesis originate in the endoplasmic reticulum (ER) and are secreted through the secretory pathway. Disruptions in ER protein homeostasis or proteostasis (i.e., ER stress) can facilitate the aberrant secretion of misfolded protein conformations to the extracellular space and exacerbate pathologic protein aggregation into proteotoxic species. Activation of an ER stress-responsive signaling pathway, the Unfolded Protein Response (UPR), restores ER proteostasis through the transcriptional regulation of ER proteostasis pathways. In contrast, the functional role for the UPR in regulating extracellular proteostasis during ER stress is poorly defined. We recently identified ERdj3 as a UPR-regulated secreted chaperone that increases extracellular proteostasis capacity in response to ER stress, revealing a previously-unanticipated direct mechanism by which the UPR impacts extracellular proteostasis. Here, we discuss the functional implications of ERdj3 secretion on extracellular proteostasis maintenance and define the mechanisms by which ERdj3 secretion coordinates intra- and extracellular proteostasis environments during ER stress.