Sensory features are encoded in topographically mapped neuronal populations in the brain. Their fine structure layout is not readily accessible due to their dense wiring and extended volume. To reveal their wiring logic, we combine genetic multicolor labeling of neural cells and large-volume micrometer scale imaging with color multiphoton microscopy. We present an analysis at single neuron resolution of the medial nucleus of the trapezoid body (MNTB), an essential relay for sound localization, which receives inputs from the cochlear nucleus (CN). Multicolor multiphoton microscopy allowed us to acquire continuous images encompassing all ~2500 MNTB neurons and CN-MNTB caliceal synapses. We traced a large portion of these afferent CN axons from their synaptic target toward their origin in the CN, and developed quantitative methods to extract various geometric properties along their trajectory. This analysis defined distinct axon domains and an abrupt transition from a collective, highly correlated and near-unidimensional trajectory to an uncorrelated, wiggly tridimensional layout. We also found that axons in the trapezoid tract were pre-ordered with respect to the arrangement of their synaptic terminals in the MNTB along the anteroposterior axis, unveiling the topographic structuration of the tract along this axis. Furthermore, single cell analysis revealed a subpopulation of caliceal axons that resists developmental synaptic elimination, resulting in convergent CN-MNTB inputs on a fraction of MNTB cells that are evenly distributed throughout most of the nucleus but form a high-density lateral hub. This raises the intriguing possibility that the MNTB may comprise distinct neuronal subpopulations encoding specific sound features or alternatively that convergence may enable to connect two unequal neuronal populations in a “no neuron left behind” model. This work provides a first single-cell resolved structure of a sensory axonal tract revealing axonal topography, trajectory and wiring patterns with individual axon precision over an entire functional area.