Disease symptom formation arises from complex interactions between a pathogen and its host. In sugarcane smut disease caused by Sporisorium scitamineum, the whip-shaped sorus—comprising intertwined fungal and plant tissues originating from the primary meristems of infected plants—is the most conspicuous symptom and a major cause of yield loss. Despite its agronomic significance, regulatory mechanisms underlying sorus development and teliospore formation remain poorly understood. This study investigated the dynamic molecular events underlying sorus morphogenesis using integrated phytohormone profiling, transcriptomics, and metabolomics. The data showed significant upregulation of auxin (IAA) and cytokinins (TZR, zeatin, and IPA) across developmental stages, with distinct spatial distribution patterns in the white, gray, and black sorus regions. Transcriptome analysis demonstrated extensive reprogramming of genes associated with phytohormone signaling—especially related to auxin, cytokinin, abscisic acid, and salicylic acid pathways—as well as genes involved in cell wall remodeling and transporter functions. Metabolomic profiling demonstrated accumulation of sucrose, raffinose, and hydroxycinnamic acids, and several organic acids peaked specifically prior to teliospore maturation. Fungal transcriptomic data highlighted strong upregulation of genes linked to hydrolase activity, transmembrane transport, and cell wall metabolism during teliospore differentiation. Furthermore, infection with RWTD1 (encoding a putative four-transmembrane domain protein)-knockout mutants impaired sorus formation and triggered host defense activation without disrupting phytohormone homeostasis. Collectively, these findings provide new insights into the coordinated phytohormonal, transcriptional, and metabolic reprogramming that mediates symptom development and teliospore formation in sugarcane smut disease.