Bladder cancer (BC), as one of the most common urological malignant tumor types worldwide, places a considerable burden on the economy and patients' health. Long non-coding RNA PGM5-AS1 has been shown to be downregulated in BC, however, its exact function in BC remains unclear. This study aimed to determine the influence of PGM5-AS1 on BC and its related mechanisms. The expression of PGM5-AS1, miR-587, and slit guided ligand 3 (SLIT3) in BC tissues and cells was detected using real-time quantitative polymerase chain reaction and Western blotting. In vitro functional experiments, including CCK-8, Transwell, and Western blotting, were used to assess BC cell proliferation, migration, and the expression of apoptosis-related proteins (Bax and Bcl-2). A xenograft tumor experiment was conducted to test the role of PGM5-AS1 in BC cell growth in vivo. In addition, the relationship between PGM5-AS1, miR-587, and SLIT3 was verified using luciferase reporter and RIP assays. PGM5-AS1 and SLIT3 were expressed at low levels in BC, whereas miR-587 exhibited the opposite trend. PGM5-AS1 overexpression significantly inhibited BC cell proliferation and migration, promoted apoptosis in vitro, and alleviated tumor growth in vivo. miR-587 has been shown to be a target of PGM5-AS1, and miR-587 overexpression can reverse the inhibitory effect of PGM5-AS1 upregulation on BC cell growth. Furthermore, miR-587 directly targeted SLIT3 and negatively regulated its expression. PGM5-AS1 inhibited BC cell proliferation and migration while facilitating apoptosis through the miR-587/SLIT3 pathway. PGM5-AS1 represses BC development via the miR-587/SLIT3 axis, indicating that PGM5-AS1 may be a candidate biomarker and target for BC treatment.