Background: Novel and recent discoveries have shown that antigen presentation to gut T cells can be carried out by gut epithelial cells in the colon. Here we show, in the inflamed stomach, that gastric epithelial cells highly express MHC-I and interact with intraepithelial CD8+ T cells, and that Absent in Melanoma 2 (Aim2) can regulate the frequency of intraepithelial CD8+ T cells. Understanding this mechanism and modulating CD8+ T cell education by gastric epithelial MHC-I can be useful in regulating the outcome of gastric pre-neoplastic and neoplastic lesions. Methods: We used a combination of methods including (1) immunofluorescence of intraepithelial E-cadherin+ CD8+ T cells in tissue sections from human gastric biopsies, (2) single-cell RNA sequencing (scRNA-Seq) of WT vs Aim2-/- 6-month H. felis-infected stomachs, (3) WT → Aim2-/- vs Aim2-/- → WT bone marrow chimeras, (3) CD19CreAim2flox/flox vs Aim2flox/flox mice, and (4) H. pylori-pulsed BMDC:T cell co-culture of WT vs Aim2-/- splenocytes. Results: Intraepithelial CD8+ T cells, which also expressed E-cadherin, were identified, by immunofluorescence, in biopsies from subjects with chronically inflamed gastric mucosae due to chronic H. pylori infection. The cell membranes of these cells were in contact with β2 microglobulin (MHC-I subunit) expressed by gastric mucous pit and neck cell membranes. In mice, MHC-I was similarly induced in gastric epithelial cells by 6-month H. felis or H. pylori infection, relative to uninfected. Intraepithelial CD8+ T cells were identified by scRNA-Seq, and they clustered with gastric epithelial cells rather than the T cell cluster, as they co-expressed a combination of CD8+ T cell and epithelial cell markers. scRNA-Seq showed that Aim2 was downregulated in these hybrid intraepithelial CD8+ T cells, relative to stromal E-cadherin- CD8+ T cells. To determine which compartment Aim2 exerts its impact on CD8+ T cells, we performed bone marrow chimera experiments (e.g., Aim2-/- → WT vs WT → Aim2-/-) followed by 6mo H. felis infection, and observed an increase in intraepithelial CD8+ T cells in Aim2-/- → WT but not WT → Aim2-/-, thus implicating a non-epithelial-intrinsic Aim2 effect. Moreover, CD19CreAim2flox/flox followed by 6mo H. felis also failed to recapitulate the Aim2 phenotype, thereby excluding B cell-intrinsic Aim2 involvement. Myeloid Aim2 involvement was also ruled out in a previous report. In contrast, CD8+ T cell-intrinsic Aim2 deficiency increased the expression of IFN-γ and tissue-resident memory T cell markers CD69 and CD103 in H. pylori-pulsed BMDC:T cell ex-vivo co-culture experiments. Conclusion: Our study suggests that intraepithelial engagement of gastric CD8+ T cells with epithelial cells may lead to downregulation of CD8 T cell Aim2 expression, thereby increasing pathogenic CD8 T cell phenotype.