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Over the past few decades, peanut smut, caused by Thecaphora frezzii, has evolved from an emerging disease to a major global threat to peanut production. However, critical knowledge gaps persist regarding the anatomical pathways and host responses involved in infection, colonization, and sporulation. This study examines the pathosystem and histopathology of the biotrophic phase of T. frezzii in the susceptible cv. Granoleico. Anatomical analyses were conducted using light microscopy, confocal laser scanning, and scanning electron microscopy. Our findings reveal that T. frezzii enters the host through the peg rather than the ovary tip, invading during the R2-subterranean phase. Fruit colonization occurs at the R3-stage when the mechanical layer between the mesocarp and endocarp has not yet formed. Hyphal entry into the seed takes place between the R3-medium and R3-late pod stages via the funiculus, leading to extensive seed coat colonization without penetrating the embryo. Once inside, hyperplasia and hypertrophy are triggered, coinciding with teliospore formation. Teliosporogenesis disrupts nutrient translocation, arresting embryo development. The hyphae colonize tissues intracellularly, utilizing living cells of the vascular bundles and following the peanut’s photoassimilate transport pathway. Investigating these structural responses in phenotypically contrasting peanut genotypes may provide key insights into the anatomical barriers and defense mechanisms that determine disease susceptibility and resistance, ultimately contributing to the development of resistant cultivars. Full article