IL-10-producing Tr1 cells promote tolerance but their contributions to tolerogenic memory are unclear. Using 10BiT mice that carry a Foxp3-eGFP reporter and stably express CD90.1 following IL-10 production, we characterized the spatiotemporal dynamics of Tr1 cells in a house dust mite model of allergic airway inflammation. CD90.1+Foxp3-IL-10+ Tr1- like cells arise from memory cells and rejoin the tissue-resident memory T-cell pool after cessation of IL-10 production. Persistent antigenic stimulation is necessary to sustain IL-10 production and Irf1 and Batf expression distinguishes CD90.1+Foxp3-IL-10+ Tr1-like cells from CD90.1+Foxp3-IL-10- “former” Tr1. Depletion of Tr1-like cells during primary challenge exacerbates allergic airway inflammation. However, neither transfer nor depletion of CD90.1+Foxp3-IL10- “former” Tr1 cells influences the inflammatory response during subsequent allergen re-challenge weeks later. Together these data suggest that naturally- arising Tr1 cells do not contribute to tolerogenic memory. This instability may limit efforts to re-establish tolerance by expanding Tr1 in vivo.