SUMMARYKRIT1, also called CCM1, is a member of a multiprotein complex that contains the products of the CCM2 and PDCD10 (also known as CCM3) loci. Heterozygous loss of any of the genes that encode these proteins leads to cerebral cavernous malformations (CCM), which are vascular lesions that are found in around 0.5% of humans. KRIT1 mediates the stabilization of β-catenin-containing endothelial cell-cell junctions downstream of the Rap1 GTPase. Here, we report that Rap1 and KRIT1 are negative regulators of canonical β-catenin signaling in mice and that hemizygous Krit1 deficiency exacerbates β-catenin-driven pathologies. Depletion of endothelial KRIT1 caused β-catenin to dissociate from vascular endothelial (VE)-cadherin and to accumulate in the nucleus with consequent increases in β-catenin-dependent transcription. Activation of Rap1 inhibited β-catenin-dependent transcription in confluent endothelial cells; this effect required the presence of intact cell-cell junctions and KRIT1. These effects of KRIT1 were not limited to endothelial cells; the KRIT1 protein was expressed widely and its depletion increased β-catenin signaling in epithelial cells. Moreover, a reduction in KRIT1 expression also increased β-catenin signaling in vivo. Hemizygous deficiency of Krit1 resulted in a ~1.5-fold increase in intestinal polyps in the ApcMin/+ mouse, which was associated with increased β-catenin-driven transcription. Thus, KRIT1 regulates β-catenin signaling, and Krit1+/− mice are more susceptible to β-catenin-driven intestinal adenomas.