Stomach adenocarcinoma (STAD) has high incidence and mortality rates. Long non-coding RNAs (lncRNAs) and angiogenesis are closely related to the pathogenesis and metastasis of STAD. Recently, emerging evidence demonstrated that DNA methylation plays crucial roles in the development of STAD. This study explored the relationship between DNA methylation and the abnormal expression of angiogenesis-related lncRNAs (ARlncRNAs) in stomach adenocarcinoma, aiming to identify prognostic biomarkers. Moreover, a Cox analysis and Lasso regression were used to establish an ARlncRNA feature set related to angiogenesis. The prognostic model was evaluated by using a Kaplan-Meier (KM) analysis, ROC curves, and nomograms. Based on the identified 18 key ARlncRNAs, a prognostic predictive model was constructed. In addition, a specific ARlncRNA with abnormal methylation in the model, LINC00511, showed significant differences in expression and methylation across different subgroups. The methylation and expression of LINC00511 were analyzed by a correlation and co-expression analysis. The correlation analysis indicated that promoter methylation may improve LINC00511 expression. Further analysis found 355 mRNAs co-expressed with LINC00511 which may interact with 6 miRNAs to regulate target gene expression. The abnormal methylation of LINC00511 could significantly contribute to the progression of stomach adenocarcinoma.