The cultural transmission of spoken language and music relies on human capacities for encoding and recalling auditory patterns. In this experiment, we show that interindividual differences in this ability are associated with variation in the organization of cross-callosal white matter pathways. First, high-angular resolution diffusion MRI (dMRI) data were analyzed in a large participant sample (N = 51). Subsequently, these participants underwent a behavioral test that models in the laboratory the cultural transmission of auditory symbolic systems: the signaling game. Cross-callosal and intrahemispheric (arcuate fasciculus) pathways were reconstructed and analyzed using conventional diffusion tensor imaging (DTI) as well as a more advanced dMRI technique: fixel-based analysis (FBA). The DTI metric of fractional anisotropy (FA) in auditory callosal pathways predicted-weeks after scanning-the fidelity of transmission of an artificial tone system. The ability to coherently transmit auditory signals in one signaling game, irrespective of the signals learned during the previous game, was predicted by morphological properties of the fiber bundles in the most anterior portions of the corpus callosum. The current study is the first application of dMRI in the field of cultural transmission, and the first to connect individual characteristics of callosal pathways to core behaviors in the transmission of auditory symbolic systems.