In eukaryotes, the retromer complex plays a crucial role in the sorting and retrograde transport of cargo proteins from endosomes to the trans-Golgi network (TGN). Despite its importance, the molecular details of this intracellular transport process remain unclear. Here, we have identified a Golgi-associated retrograde protein (GARP) complex as a mediator of vesicle transport that facilitates the recruitment of the retromer complex to the TGN to exert its functions. The GARP complex is mainly localized in the TGN where it interacts with the retromer complex. This interaction is evolutionarily conserved across species. Furthermore, we identified FgKex2 and FgSnc1 as cargo proteins in the GARP/retromer-mediated recycling pathway. Loss of GARP or retromer results in a complete missorting of FgKex2 and FgSnc1 into the vacuolar degradation pathway, which affects the growth, development, biogenesis of toxisomes and pathogenicity of Fusarium graminearum. In summary, we demonstrate for the first time that GARP promotes the recruitment of retromer from endosomes to the TGN, thereby establishing a GARP/retromer transport pathway that coordinates the recycling of cargo proteins FgKex2 and FgSnc1. This process is essential for maintaining sustained growth and development and significantly contributes to the pathogenicity of F. graminearum.