Endoglin (Eng) is an auxiliary receptor for TGFβ with important roles in vascular function. TGFβ regulates angiogenesis through balancing the pro-proliferative and pro-differentiation signaling pathways of endothelial cells (EC). However, the contribution of endoglin to these TGFβ activities, and more specifically modulation of EC phenotype remain elusive. Mutations in endoglin cause hereditary hemorrhagic telangiectasia-1 in humans. The Eng +/− mice are viable and exhibit some of the vascular defects seen in humans with endoglin haploinsufficiency. Here we show that haploinsufficiency of endoglin resulted in attenuation of retinal neovascularization during oxygen-induced ischemic retinopathy. Although the importance of endoglin expression in angiogenesis and vascular development has been demonstrated the underlying mechanisms remain obscure. To gain detailed insight into the cell autonomous regulatory mechanisms which impact angiogenic properties of EC, we prepared retinal EC from Eng+/+ and Eng+/− Immorto mice. The Eng +/− EC were more adherent, less migratory, and failed to undergo capillary morphogenesis. Aortic sprouting angiogenesis was similarly attenuated in aortas from Eng +/− mice. In addition, Eng +/− EC expressed increased levels of VEGF but reduced expression of endothelial nitric oxide synthase and NO production. Mechanistically, these changes were consistent with sustained activation of MAPK pathways, and aberrant Smad-dependent signaling pathways in Eng +/− EC. Together our results underscore the importance of endoglin in both canonical and non-canonical TGFβ signaling pathways modulating both the activation and quiescence of the endothelium during angiogenesis.