Irritant contact dermatitis (ICD) is a common inflammatory skin disease caused by direct exposure to exogenous irritants, characterized by skin barrier disruption and persistent inflammation. Here, we developed a 169-well hanging-drop platform for the uniform and scalable generation of human follicle dermal papilla cell (HFDPC)-derived organoids. The honeycomb-shaped microwell array promoted gravity-driven cellular aggregation and controlled organoid formation, while Matrigel provided an extracellular matrix (ECM)-rich three-dimensional (3D) microenvironment supporting tissue-like organization. Compared with conventional Matrigel-based culture, the proposed platform enabled improved control of organoid size and morphology, reproducible formation, and high-throughput production. The platform generated highly uniform organoids with a mean diameter of 116.55 ± 4.36 μm (mean ± SD) and a coefficient of variation of 3.74%, while integration with a standard 6-well plate enabled simultaneous production of up to 1014 organoids. In an ICD mouse model, transplantation of the organoids accelerated skin repair and alleviated inflammation, accompanied by reduced oxidative stress, restored SirT1 expression, attenuated PI3K/AKT phosphorylation, and suppressed Th1/Th17-mediated immune responses. These findings indicate that the combination of a 169-well hanging-drop architecture with a Matrigel-based 3D microenvironment provides a controlled and scalable platform for HFDPC organoid generation, with therapeutic potential demonstrated in an ICD mouse model.