Pancreatic cancer (PC) is among the most notorious malignancies worldwide. Long noncoding RNA (IncRNA) repulsive guidance molecule bone morphogenetic protein (BMP) coreceptor b antisense RNA 1 (RGMB-AS1) was an oncogene in glioma. However, the RGMB-AS1 function in PC remains largely unknown. Herein, quantitative real-time polymerase chain reaction was performed to analyze the expression of RGMB-AS1. We determined RGMB-AS1 influence on PC cell malignant behaviors via functional assays. Besides, we applied subcellular fractionation and fluorescence in situ hybridization (FISH) assays to confirm the cellular distribution of RGMB-AS1 in PC cells. We used mechanism assays to detect the regulatory axis of RGMB-AS1 in PC cells. Briefly, the level of RGMB-AS1 expression in PC cells was abnormally high. RGMB-AS1 knockdown impeded PC cell proliferation and migration, but induced cell apoptosis, and RGMB-AS1 overexpression led the opposite consequences. RGMB-AS1 acted as a competing endogenous RNA (ceRNA) to sequester miR-574-3p and thereby regulated Pim-3 proto-oncogene, serine/threonine kinase (PIM3) expression. Conclusively, our work revealed the cancer-promoting function of RGMB-AS1 in PC and that the regulatory mechanism of the RGMB-AS1/miR-574-3p/PIM3 axis might contribute to novel biomarker development in PC treatment. NEW & NOTEWORTHY RGMB-AS1 promotes PC cell proliferation, elevates PC cell migration capacity, inhibits PC cell apoptosis, and promotes PC cell proliferation and migration but inhibits cell apoptosis via targeting miR-574-3p. PIM3 is directly targeted by miR-574-3p.