Vascular morphogenesis requires the complementary processes of vasculogenesis, angiogenesis and arteriogenesis. All three processes are VEGF-A dependent, but how VEGF-A signalling is regulated to selectively stimulate each one at the appropriate time is poorly understood. The VEGF-A isoform specific receptor neuropilin 1 (NRP1) contributes to both angiogenesis and arteriogenesis and has additionally been implicated in vascular permeability. We find that mice expressing solely a truncated form of NRP1 lacking the cytoplasmic domain have normal angiogenesis. In contrast, they show reduced arteriogenesis, similar to mice lacking synectin/GIPC1, which binds the NRP1 cytoplasmic domain. Tissue culture studies linked the arteriogenic defect to impaired VEGFR2 endocytosis downstream of VEGF-A activation, which increased dephosphorylation of the VEGFR2 site that activates ERK1/2 signalling. Mice lacking the NRP1 cytoplasmic tail also showed reduced VEGF-A induced vascular permeability, but, synectin was not required for the permeability response. Taken together, these findings suggest that the membrane-anchored extracellular domain of NRP1 is sufficient for angiogenesis, whilst arteriogenesis and vascular permeability additionally require the NRP1 cytoplasmic tail, with a differential dependence on synectin.