Mitogens trigger cell division in animals. In plants, cytokinins, a group of phytohormones derived from adenine, stimulate cell proliferation. Cytokinin signaling is initiated by membrane-associated histidine kinase receptors and transduced through a phosphorelay system. Here we show, in the Arabidopsis shoot apical meristem (SAM), that cytokinin regulates cell division by promoting nuclear shuttling of Myb-domain protein 3R4 (MYB3R4), a transcription factor that activates mitotic gene expression. Newly synthesized MYB3R4 protein resides predominantly in the cytoplasm. At the G2/M transition, rapid nuclear accumulation of MYB3R4—consistent with an associated transient peak in cytokinin concentration—feeds a positive-feedback loop involving importins, and initiates a transcriptional cascade that drives mitosis and cytokinesis. An engineered nuclear-restricted MYB3R4 mimics the cytokinin effects in enhancement of cell proliferation and meristem growth.