Abstract Background LncRNAs are critical regulators of bladder cancer (BLCA), and ferroptosis is a newly discovered cell death responsible for mediating apoptosis and tumorigenesis. The present study aims to establish a prognostic signature of differentially expressed ferroptosis-related lncRNAs (DEFRlncRNAs) and explore the DEFRlncRNA associated with NUPR1 in BLCA. Methods DEFRlncRNAs in BLCA patients were screened using univariate and multivariate Cox and LASSO regression analyses. In vitro experiments were performed to detect the regulatory effects of DEFRlncRNAs on BLCA cells. A prognostic signature of DEFRlncRNAs in BLCA was created and validated. Moreover, we used RNA-binding protein immunoprecipitation (RIP) to evaluate the correlated DEFRlncRNA with NUPR1. Results A prognostic signature involving 18 DEFRlncRNAs in BLCA was created. Overexpression of AL355353.2 or knockdown of AL136084.3 promoted apoptosis in 5637 and T24 cells in vitro. Results from Starbase database estimated that AL136084.3 was positively associated with NUPR1 (R = 0.229, p