Introduction: Cardiometabolic HFpEF is characterized by T cell systemic inflammation and can be modeled preclinically with high fat diet (HFD) and L-NAME. Metabolic perturbations can alter T cell function through modulation of the unfolded protein response (UPR). How T cells are activated in HFpEF and whether T cell inflammation can be tuned by removing cardiometabolic stress remains unknown. Hypothesis: HFD and L-NAME induce reversible alterations in T cell UPR signaling that modulate T cell dependent cardiac inflammation and pathology in experimental HFpEF. Methods: Male C57/BL6J mice (wild-type, WT), OT-II antigen restricted mice, and CD4 Cre Xbp1 fl/fl mice were fed a high-fat diet (HFD) and L-NAME (H/L) for 5 weeks. WT mice were switched to standard diet (STD) for two additional weeks. WT mice receiving HFD or L-NAME only, or TAC surgery (a model of HF with reduced EF) were used as controls. Left ventricular (LV) end diastolic pressure volume relationship (EDPVR) was assessed using invasive hemodynamic analyses and LV EF by echocardiography. Cardiac and splenic T cells were characterized by flow cytometry and T cell UPR was evaluated by qPCR and Western blot. Results: 5 weeks of H/L was sufficient to induce cardiac T cell infiltration and splenic T cell activation. OTII mice fed H/L showed increased cardiac CD4 + T cell infiltration compared to STD controls, indicating T cell activation is not cardiac antigen restricted. Furthermore, splenic T cell characterization revealed H/L resulted in decreased phosphorylation of the UPR protein inositol-requiring enzyme 1α (IRE1α) and reduced expression of X box-binding protein 1 ( Xbp1s/u ) compared to T cells from mice exposed to HFD or L-NAME alone, STD, or WT TAC controls. CD4 Cre+ Xbp1 fl/fl mice (T cell Xbp1 -/- ) fed with H/L had increased cardiac T cell infiltration compared to Cre - controls. Lastly, Xbp1s expression in splenic CD4 + T cells was recovered after withdrawal of H/L and resulted in partial reduction of cardiac hypertrophy, decreased EDPVR, as well as less cardiac T cell infiltration compared to mice kept on H/L. Conclusions: Reversible downregulation of the T cell IRE1α-XBP1 axis is a unique T cell signature of HFpEF that contributes to T cell inflammation and adverse cardiac remodeling.