Alanylglutamine (AG) is a dipeptide that acts as a coadjuvant during gut healing by fueling enterocytes. The current study sought to look into AG’s possible ulcer-healing properties in indomethacin-induced gastropathy. Five groups of animals were assigned at random. Following indomethacin exposure, gastric ulcerated rats were given AG, AG with dexamethasone, or pantoprazole. AG blocked the H+-K+ATPase pump and raised the pH of gastric juice in the same way that pantoprazole did. The dipeptide also enhanced the serum/mucosal levels of glucagon-like peptide-1 (GLP-1), pS473-Akt, and cyclin-D1. AG, on the other hand, reduced blood tumor necrosis factor-α and gastric mucosal levels of pS9-GSK3β, pS133-CREB, pS536-NF-κB, H2O2, claudin-1, and caspase-3 content. Dexamethasone dosing prior to AG impeded its effect on nearly all of the assessed measures. AG confers its antiulcerogenic/antisecretory properties by suppressing the proton pump, which raises the pH of the gastric juice by increasing p-CREB, p-Akt, p-GSK-3β, and GLP-1 levels. It also suppresses apoptosis by inhibiting the nuclear factor-kappa B/tumor necrosis factor-α/H2O2/claudin-1 cue.