CAPRIN1, cell cycle–associated protein 1, is an RNA-binding protein in stress granules, P bodies, and messenger RNA transport granules and has a high level of expression in cancer. It promotes the proliferation and invasion of cancer cells and enhances their glycolysis and chemoresistance. In addition, it mediates the formation of intracellular SGs in various ways when exposed to endogenous and exogenous stress. As an RNA-binding protein, it not only directly binds to several mRNAs associated with the cell cycle but also is the target of miRNA, lncRNA, and circRNA. Recently, CAPRIN1 is identified as a phase-separating protein that mediates the liquid–liquid phase separation within tumor cells. Moreover, the formation of CAPRIN1-mediated phase separation is regulated by circRNA and lncRNA. In addition, CAPRIN1 is associated with ubiquitination, which affects the relevant characteristics of cancer cells. This review discusses the different regulatory mechanisms of CAPRIN1 in various tumors and its association with noncoding RNA, suggesting its potential as an oncogenic signal and possibly as a diagnostic indicator in the future. This may provide the multifunctional characteristic insight of CAPRIN1 protein and potential therapeutic target in malignancy with high levels of CAPRIN1.