This study profiles 421,312 individual cells from the esophageal mucosa of 7 healthy and 15 eosinophilic esophagitis (EoE) participants, revealing 60 cell subsets and functional alterations in cell states, compositions, and interactions. Active EoE is characterized by enriched *ALOX15* macrophages, *PRDM16* dendritic cells expressing the EoE risk gene *ATP10A*, and cycling mast cells, with a reduction in T_H17 cells. Ligand-receptor expression identifies eosinophil recruitment programs, increased fibroblast interactions, and IL-9^IL-4IL-13<sup>T</sub>__H2 and endothelial cells as potential mast cell interactors. Remission is marked by contraction of mast and CD4⁺T_RM cells and downregulation of eosinophil chemoattractant, growth, and survival factors. These findings advance our understanding of EoE and provide opportunities for therapeutic intervention.This study profiles 421,312 individual cells from the esophageal mucosa of 7 healthy and 15 eosinophilic esophagitis (EoE) participants, revealing 60 cell subsets and functional alterations in cell states, compositions, and interactions. Active EoE is characterized by enriched *ALOX15* macrophages, *PRDM16* dendritic cells expressing the EoE risk gene *ATP10A*, and cycling mast cells, with a reduction in T_H17 cells. Ligand-receptor expression identifies eosinophil recruitment programs, increased fibroblast interactions, and IL-9^IL-4IL-13<sup>T</sub>__H2 and endothelial cells as potential mast cell interactors. Remission is marked by contraction of mast and CD4⁺T_RM cells and downregulation of eosinophil chemoattractant, growth, and survival factors. These findings advance our understanding of EoE and provide opportunities for therapeutic intervention.