Characterizing blood flow dynamics in vivo is critical to understand the function of vascular network under physiological and pathological conditions. Existing methods for hemodynamic imaging have insufficient spatial and temporal resolution to monitor blood flow at cellular level in large blood vessels. By employing an ultrafast line-scanning module based on free-space angular chirped enhanced delay (FACED), we achieved two-photon fluorescence imaging of cortical blood flow at 1,000 2D frames and 1,000,000 1D line scans per second in the awake mouse. This orders-of-magnitude increase in temporal resolution allowed us to measure cerebral blood flow up to 49 mm/s and observe pulsatile blood flow at harmonics of heart rate. Directly visualizing red blood cell (RBC) flow through vessels down to >800 µm in depth, we characterized cortical-layer-dependent flow velocity distributions of capillaries, obtained radial velocity profiles and kilohertz 2D velocity mapping of multi-file blood flow, and carried out RBC flux measurements from penetrating blood vessels.