Psoriasis is a common chronic inflammatory skin disease with no cure. It is driven by the interleukin (IL)-23/IL-17A axis and type 17 T helper cells; however, recently, group 3 innate lymphoid cells (ILC3s) have also been implicated. Despite being the focus of much research, factors regulating the activity of ILC3s remain incompletely understood. Immune regulatory pathways are particularly important at barrier sites, such as the skin, gut, and lungs, which are exposed to environmental substances and microbes. CD200R1 is an immune regulatory cell surface receptor that inhibits proinflammatory cytokine production in myeloid cells. CD200R1 is also highly expressed on ILCs, where its function remains largely unexplored. We previously observed reduced CD200R1 signaling in psoriasis-affected skin, suggesting that dysregulation may promote disease. Here, we show that contrary to this, psoriasis models are less severe in CD200R1-deficient mice due to reduced IL-17 production. Here, we uncover a key cell-intrinsic role for CD200R1 in promoting IL-23-driven IL-17A production by ILC3s by promoting signal transducer and activator of transcription 3 activation. Therefore, contrary to its inhibitory role in myeloid cells, CD200R1 is required on ILC3 to promote IL-23-stimulated signal transducer and activator of transcription 3 activation, triggering optimal IL-17 production.