In recent years, the field of functional neuroimaging has moved from a pure localisationist approach of isolated functional brain regions to a more integrated view of those regions within functional networks. The methods used to investigate such networks, however, rely on local signals in grey matter and are limited in identifying anatomical circuitries supporting the interaction between brain regions. Mapping the brain circuits mediating the functional signal between brain regions would propel forward our understanding of the brain’s functional signatures and dysfunctions. We developed a novel method to unravel the relationship between brain circuits and functions: The Functionnectome. The Functionectome combines the functional signal from fMRI with the anatomy of white matter brain circuits to unlock and chart the first maps of functional white matter. To showcase the versatility of this new method, we provide the first functional white matter maps revealing the joint contribution of connected areas to motor, working memory, and language functions. The Functionnectome comes with an open source companion software and opens new avenues into studying functional networks by applying the method to already existing dataset and beyond task fMRI.