The atypical cadherin FAT4 has established roles in the regulation of planar cell polarity and Hippo pathway signaling that are largely dependent on cell context. The recent identification of FAT4 mutations in Hennekam syndrome, features of which include lymphedema, lymphangiectasia, mental retardation and unusual facial morphology, uncovered an important role for FAT4 in the lymphatic vasculature. Hennekam syndrome also arises due to mutations in CCBE1 and ADAMTS3, encoding a matrix protein and protease, respectively, that regulate activity of the key pro-lymphangiogenic VEGF-C/VEGFR3 signaling axis by facilitating the proteolytic cleavage and activation of VEGF-C. The fact that FAT4, CCBE1 and ADAMTS3 mutations underlie Hennekam syndrome suggests that all three genes might function in a common pathway. We identified FAT4 as a direct target gene of GATA2, a key transcriptional regulator of lymphatic vascular development and in particular, valve development. Here, we demonstrate that FAT4 functions in a lymphatic endothelial cell autonomous manner to control cell polarity and is required for lymphatic vessel morphogenesis throughout development. Moreover, we demonstrate that loss of FAT4 function impacts VEGF-C induced VEGFR3 signaling, not as a result of controlling proteolytic activation of VEGF-C, but by regulating signaling downstream of VEGFR3 activation. Together, our data reveal a crucial role for FAT4 in lymphangiogenesis and shed light on the mechanistic basis by which FAT4 mutations underlie a human lymphedema syndrome.