Idiopathic pulmonary fibrosis (IPF), one of the most common forms of interstitial lung disease, is a poorly understood and fatal condition with only two FDA-approved medications. As a chronic fibroproliferative disorder, the pathobiology of the fibroblast in IPF is critical to the evaluation and discovery of novel therapeutics. Unfortunately, our ability to interrogate this biology in vitro is greatly limited by the well-documented effect of tissue culture plastic on the fibroblast phenotype. Using decellularized IPF-derived lung matrix, we characterize the phenotype of fibroblasts seeded into three-dimensional (3D) fibrotic hydrogels. We identify differential gene expression and differential contractility in IPF fibroblasts as compared to their normal counterparts. Additionally, fibroblasts seeded into these matrices lose the classical myofibroblast marker, smooth muscle actin, and gain significant expression of proinflammatory cytokines compared to 2D tissue culture dishes. In a series of co-culture studies with monocytes and monocyte- derived macrophages, we validate this proinflammatory state. The application of this 3D fibrotic hydrogel model for the potential intervention in disease associated fibroblast-immune cell crosstalk may uncover a novel therapeutic avenue. These findings add to a growing understanding of the lung microenvironment effect on fibroblast phenotypes and shed new light on the potential role of fibroblasts as immune signaling hubs during lung fibrosis.