Long noncoding RNAs (lncRNAs) are emerging as critical regulators for cancer pathogenesis, yet their pan-cancer expression landscapes and functional mechanisms remain to be defined. Through the first systematic analysis of lncRNA expression across 20 cancer types using TCGA transcriptomic data, we identified MILIP as a c-Myc–inducible lncRNA upregulated in 18 cancer types. Functional studies demonstrated that MILIP promoted cancer cell proliferation and survival, and high MILIP levels were correlated with poor patient survival, supporting its pan-cancer oncogenic role. Mechanistically, in p53 wildtype cancers, MILIP acted as a p53 inhibitor by directly binding to p53, competitively blocking TRIML2-mediated SUMOylation, and promoting p53 polyubiquitination and degradation. In p53 mutant cancers, MILIP instead promoted protein synthesis by forming a ternary complex with eEF1a1 and type II tRNAs, facilitating tRNA loading onto eEF1a1. Therapeutic silencing of MILIP using Gapmer suppressed tumor growth in vivo. Together, these findings uncover a dual mechanistic role for MILIP in cancer pathogenesis and highlight its potential as a therapeutic target in both p53 wildtype and mutant tumors.