In plants, WUSCHEL-related homeobox1 (WOX1) homologs promote lamina mediolateral outgrowth. However, the downstream components linking WOX1 and lamina development remain unclear. In this study, we revealed the roles of WOX1 in palmate leaf expansion in cucumber (Cucumis sativus). A cucumber mango fruit (mf) mutant, resulting from truncation of a WOX1-type protein (CsWOX1), displayed abnormal lamina growth and defects in the development of secondary and smaller veins. CsWOX1 was expressed in the middle mesophyll and leaf margins and rescued defects of the Arabidopsis wox1 prs double mutant. Transcriptomic analysis revealed that genes involved in auxin polar transport and auxin response were highly associated with leaf development. Analysis of the cucumber mf rl (round leaf) double mutant revealed that CsWOX1 functioned in vein development via PINOID (CsPID1)-controlled auxin transport. Overexpression of CsWOX1 in cucumber (CsWOX1-OE) affected vein patterning and produced ‘butterfly-shaped’ leaves. CsWOX1 physically interacted with CsTCP4a, which may account for the abnormal lamina development in the mf mutant line and the smaller leaves in the CsWOX1-OE plants. Our findings demonstrated that CsWOX1 regulates cucumber leaf vein development by modulating auxin polar transport; moreover, CsWOX1 regulates leaf size by controlling CIN-TCP genes.