Olfaction is involved in detecting, identifying, and discriminating dietary fat within foods, yet the underlying neural mechanisms remain uncharted. Our fMRI study investigated the neural correlates of olfactory fat perception and their association with discrimination ability in a complex food matrix. We measured brain activation resulting from orthonasal exposure to an ecologically relevant fat-related odour source - dairy milk, manipulated to contain 0%, 3.5% or 14% fat. Twenty-six healthy, normosmic adults underwent olfactory fat content discrimination testing, followed by an fMRI task during which the three odour stimuli were delivered via an olfactometer (25 times/fat level) and rated on perceived intensity and liking. Participants discriminated between all fat levels, with fat level influencing perceived odour intensity and liking. These perceptual differences, however, were not reflected in differential brain activation. Brain activation differences were observed only when comparing odour exposure with no exposure. Specifically, in response to any odour, activation occurred in the anterior part of the supplementary motor area, while deactivating parts of the hippocampus, putamen, superior temporal gyrus, anterior cingulate cortex, insula and posterior part of the supplementary motor area. Exposure to the 0% fat odour also activated the thalamus. No associations were found between perceived intensity and liking and neural responses. Results reaffirm the human ability to distinguish food fat content using solely olfactory cues and reveal a divergence between sensory perception and neural processing. Subsequent research should replicate and extend these findings onto retronasal fat perception, while also examining potential effects of hunger, genetics, and dietary habits.