A comprehensive technique was developed for using three-dimensional ¹⁷O magnetic resonance spectroscopic imaging at 9.4T for rapidly imaging the cerebral metabolic rate of oxygen consumption (CMRO₂) in the rat brain during a two-min inhalation of ¹⁷O₂. The CMRO₂ value (2.19 ± 0.14 μmol/g/min, n = 7) was determined in the rat anesthetized with α-chloralose by independent and concurrent ¹⁷O NMR measurements of cerebral H₂¹⁷O content, arterial input function, and cerebral perfusion. CMRO₂ values obtained were consistent with the literature results for similar conditions. Our results reveal that, because of its superior sensitivity at ultra-high fields, the ¹⁷O magnetic resonance spectroscopic imaging approach is capable of detecting small dynamic changes of metabolic H₂¹⁷O during a short inhalation of ¹⁷O₂ gas, and ultimately, for imaging CMRO₂ in the small rat brain. This study provides a crucial step toward the goal of developing a robust and noninvasive ¹⁷O NMR approach for imaging CMRO₂ in animal and human brains that can be used for studying the central role of oxidative metabolism in brain function under normal and diseased conditions, as well as for understanding the mechanisms underlying functional MRI.