The transcriptional repressor Capicua (Cic) controls tissue patterning and restricts organ growth, and has been recently implicated in several cancers. Cic has emerged as a primary sensor of signaling downstream of the receptor tyrosine kinase (RTK)/extracellular signal-regulated kinase (ERK) pathway, but how Cic activity is regulated in different cellular contexts remains poorly understood. We found that the kinase Minibrain (Mnb, ortholog of mammalian DYRK1A), acting through an adaptor protein Wings apart (Wap), physically interacts with and phosphorylates the Cic protein. Mnb and Wap inhibit Cic function by limiting its transcriptional repressor activity. Downregulation of Cic by Mnb/Wap is necessary for promoting the growth of multiple organs, including the wings, eyes, and the brain, and for proper tissue patterning in the wing. We have thus uncovered a previously unknown mechanism of downregulation of Cic activity by Mnb and Wap. This mechanism operates in parallel to ERK-dependent control of Cic, indicating that Cic functions as an integrator of upstream signals that are essential for tissue patterning and organ growth. Finally, since DYRK1A and CIC exhibit, respectively, pro-oncogenic versus tumor suppressor activities in human oligodendroglioma, our results raise the possibility that DYRK1A may also downregulate CIC in human cells.