YBX1 (Y box binding protein 1) is an RNA-/DNA-binding multifunctional protein harboring the classical cold shock protein (CSD) domain, an A/P domain, and a long C-terminal domain with alternating positively and negatively charged amino acids. It is a well-established oncogenic transcriptional factor, and regulates apoptosis, translation, cell proliferation, mRNA splicing, repair, differentiation, and stress response. The non-coding transcriptome has added yet another layer of complexity to the YBX1-mediated master regulation of cellular functions. Interestingly, YBX1 has been shown to localize to cytoplasmic granules such as P granules and stress granules. These granules regulate the non-coding transcriptome profile as well as mRNA translation and degradation. In this review, we discuss the recent findings on YBX1 signaling as mediated by various classes of non-coding RNAs, and on the functions of YBX1 at P granules, stress granules, exosomes, and mitochondria. YBX1 is a well-established target for cancer therapy and understanding its functions at organelles and ncRNA transcriptomes will shed new insights for devising organelle based anti-cancer therapies.