Gliomas are one the most prevalent malignant carcinomas of the central nervous system, and angiogenesis plays a critical role in the progression of these blood vessel-rich tumors. HOTAIR, a long non-coding RNA (lncRNA), acts as an oncogene in gliomas; however, its role in glioma angiogenesis remains unclear. In the present study, we identified a pro-angiogenic activity of HOTAIR. Silencing HOTAIR inhibited glioma-induced endothelial cell proliferation, migration, and tube formation. Further studies showed that vascular endothelial growth factor A (VEGFA) was involved in the HOTAIR-induced glioma angiogenesis. Our study also showed that HOTAIR was present in the glioma cell culture supernatant and was protected by membranes, suggesting that HOTAIR may affect glioma angiogenesis not only via regulation of VEGFA expression in the glioma cells, but also by transmission into endothelial cells via glioma cell-derived extracellular vesicles.