Nucleoli are well defined for their function in ribosome biogenesis, but only a small fraction of the nucleolar proteome has been characterized. Here, we report that the proto‐oncogene, c‐Jun, is targeted to the nucleolus. Using live cell imaging in myogenic cells, we document that the c‐Jun basic domain contains a unique, evolutionarily conserved motif that determines nucleolar targeting. Fos family Jun dimer partners, such as Fra2, while nuclear, do not co‐localize with c‐Jun in the nucleolus. A point mutation in c‐Jun that mimics Fra2 (M260E) in its Nucleolar Localization sequence (NoLS) results in loss of c‐Jun nucleolar targeting while still preserving nuclear localization. Fra2 can sequester c‐Jun in the nucleoplasm, indicating that the stoichiometric ratio of heterodimeric partners regulates c‐Jun nucleolar targeting. Finally, nucleolar localization of c‐Jun modulates nucleolar architecture and ribosomal RNA accumulation. These studies highlight a novel role for Jun family proteins in the nucleolus, having potential implications for a diverse array of AP‐1‐regulated cellular processes.