The cerebral windkessel is the suppression of the arterial pulse in the cranium which renders capillary blood flow smooth. Arterial pressure and flow are normally synchronous, and (counterintuitively) the intracranial pressure (ICP) pulse slightly precedes the arterial blood pressure (ABP) pulse. Transfer function analysis of the ABP pulse to the ICP pulse shows a local minimum of amplitude response (a notch) at the heart rate, and abnormal intracranial dynamics attenuates the notch and shifts phase. I propose that these counterintuitive aspects of intracranial pulsatility may be understood by treating the cerebral windkessel as a designed system. On that basis, I here apply principles of reverse-engineering to model the ICP pulse first as a simple harmonic oscillator, then as a forced harmonic oscillator with one or two degrees of freedom. By including a model of the intra- and extra-capillary pathways, I show that ABP-ICP dynamics are characteristic of a dynamic pulsation absorber—a system of vibration suppression widely used in engineering. MRI flow imaging shows that this is accomplished by an arterial-cerebrospinal fluid (CSF)-venous pump. During systole, CSF links arterial expansion to venous compression. During diastole, CSF links venous expansion to arterial relaxation. Arterial pulsations pass through the CSF to the veins, and this transposition of the arterial pulse by venous compression and relaxation provides an elastic force that continuously opposes the radial motion of the capillary walls. This maintains the resonant dynamics necessary for efficient perfusion and the anti-resonant dynamics necessary for capillary protection. Maintenance of anti-resonant dynamics (crucial for preventing cerebral edema and capillary damage) requires a system of autoregulation of intracranial pulsatility, which the cerebral windkessel provides.