Dicotyledonous plants form an apical hook to protect the fragile apical meristem during upward protrusion from the soil. Etiolated pifq (pif1 pif3 pif4 pif5) seedlings display constitutive apical hook opening. Here, we show that PIF proteins control apical hook opening by regulating the expression of Budding Uninhibited by Benzimidazole 3.1 (BUB3.1) and affecting cytokinesis. Consistent with the major function of BUB3.1 in the organization of phragmoplasts during cytokinesis, the phragmoplasts are well formed in dark-grown pifq but not in wild type. DNA staining and flow cytometry analysis further demonstrate that cellular endoreduplication levels are dramatically reduced in pifq. Chemical treatment with caffeine, an inhibitor of phragmoplast-based cytokinesis, shows that cytokinesis is involved in the apical hook opening. Genetically, BUB3.1 is epistatic to PIFq in the regulation of cytokinesis. Our findings reveal an organ-specific role of PIF proteins in regulating cytokinesis by BUB3.1 during apical hook development.