Members of the Regulator of G-protein signaling (Rgs) family regulate the extent and timing of G protein signaling by increasing the GTPase activity of Gα protein subunits. The Rgs family memberRgs1is one of the most up-regulated genes in tissue-resident memory (T_RM) T cells when compared to their circulating T cell counterparts. Functionally, Rgs1 preferentially deactivates Gαq, and Gαi protein subunits and can therefore also attenuate chemokine receptor-mediated immune cell trafficking. The impact ofRgs1expression on tissue-resident T cell generation, their maintenance, and the immunosurveillance of barrier tissues, however, is only incompletely understood. Here we report that Rgs1 expression is readily induced in naïve OT-I T cellsin vivofollowing intestinal infection withListeria monocytogenes-OVA. In bone marrow chimeras,Rgs1^-/-andRgs1^+/+T cells were generally present in comparable frequencies in distinct T cell subsets of the intestinal mucosa, mesenteric lymph nodes, and spleen. After intestinal infection withListeria monocytogenes-OVA, however, OT-IRgs1^+/+T cells outnumbered the co-transferred OT-IRgs1^-/-T cells in the small intestinal mucosa already early after infection. The underrepresentation of the OT-IRgs1^-/-T cells persisted to become even more pronounced during the memory phase (d30 post-infection). Remarkably, upon intestinal reinfection, mice with intestinal OT-IRgs1^+/+T_RMcells were able to prevent the systemic dissemination of the pathogen more efficiently than those with OT-IRgs1^-/-T_RMcells. While the underlying mechanisms are not fully elucidated yet, these data thus identifyRgs1as a critical regulator for the generation and maintenance of tissue-resident CD8⁺T cells as a prerequisite for efficient local immunosurveillance in barrier tissues in case of reinfections with potential pathogens.