Ischaemic stroke is a leading cause of death and disability. Circulating extracellular vesicles (EVs) post-stroke may help brain endothelial cells (BECs) counter ischaemic injury. However data on how EVs from ischaemic stroke patients, considering injury severity, affect these cells are limited. The aims were to characterize the inflammatory and angiogenic components of circulating EVs in acute ischaemic stroke patients, considering stroke severity, and to investigate whether these circulating EVs differentially influence the proangiogenic properties and blood-brain barrier (BBB) integrity of human BECs. Eighteen ischaemic stroke patients (acute phase: 24-48 h) and nine controls matched by age, sex, and blood pressure were studied. Stroke severity was classified as severe (n = 9) or mild (n = 9). Plasma EVs were analysed for size, concentration, and protein markers (CD63, Alix, CD81, TSG101, HSP70), as well as proinflammatory and angiogenic proteins. EV uptake, cell viability, proangiogenic capacity, electrical resistance [TEER (transendothelial electrical resistance)], and dextran-70 kD permeability were assessed using human brain microvascular endothelial cells (hCMEC/D3). Stroke patients had lower EV concentrations than controls (p = 0.075), with mild-stroke patients having the smallest EVs. Stroke-derived EVs had higher levels of interleukin 6 (IL-6), tumour necrosis factor alpha (TNF-alpha), nitrotyrosine, and vascular endothelial growth factor (VEGF) but lower placental growth factor (PLGF) compared to controls. IL-6 was higher in mild strokes (p = 0.0025), and VEGF was higher in severe strokes (p = 0.048). EVs from severe-stroke cases enhanced proangiogenic capacity and minimally disrupted the BBB. Stroke severity influences EV number, size, and composition. EVs from severe strokes may promote BBB restoration and cerebral angiogenesis, suggesting their role in intercellular communication and homeostasis in ischaemic tissue.