The immunopathogenesis of psoriasis, a common chronic inflammatory disease of the skin, is incompletely understood. Here we demonstrate, using a combination of single cell and spatial RNA sequencing, IL-36 dependent amplification of IL-17A and TNF inflammatory responses in the absence of neutrophil proteases, which primarily occur within the supraspinous layer of the psoriatic epidermis. We further show that a subset ofSFRP2+fibroblasts in psoriasis contribute to amplification of the immune network through transition to a pro-inflammatory state. TheSFRP2+fibroblast communication network involves production ofCCL13,CCL19andCXCL12, connected by ligand-receptor interactions to other spatially proximate cell types:CCR2+myeloid cells,CCR7+LAMP3+dendritic cells, andCXCR4expressed on both CD8+Tc17 cells and keratinocytes, respectively. TheSFRP2+fibroblasts also express cathepsin S, further amplifying inflammatory responses by activating IL-36G in keratinocytes. These data provide an in-depth view of psoriasis pathogenesis, which expands our understanding of the critical cellular participants to include inflammatory fibroblasts and their cellular interactions.