The Volcán de Colima is one of the most active volcanoes in North America, but it still has a poorly constrained upper crustal structure. We used ambient seismic noise tomography to generate the highest-resolution three-dimensional shear-wave velocity model of the volcano to date. We measured group velocity dispersion curves of Rayleigh and Love waves extracted from the records of two distinct networks deployed on the Colima Volcanic Complex. Those were regionalized into 2-D velocity maps and then locally inverted using a neighborhood algorithm and an anisotropic parametrization to obtain an accurate shear-velocity model down to 4 km below sea level. The resulting model highlights a network of deeply rooted NE-SW low-velocity zones oriented along a local fault system. This low-velocity zone also roughly aligns with the north-south trend associated with the gradual trenchward shift of the magmatic front of the quaternary Colima Volcanic Complex. An overlapping negative radial anisotropy indicates that magma follows vertically oriented structures, such as interfingered dikes, faults, or cracks with a substantial vertical component. Our results also highlight the difference between the former active system, filled with solidified dikes and sills, and the current one, associated with a network of fluid-filled dikes.