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This study aimed to explore transcriptomic distinctions between resistant (CS‐319) and susceptible (JAL‐42) groundnut (Arachis hypogaea) genotypes exposed to Sclerotium rolfsii infection across different developmental stages. Employing a de novo assembly‐based approach, we analysed the transcriptomic response in these groundnut plants under control and infected conditions at 24, 72 and 120 hours post‐inoculation (hpi). Our RNA‐Seq data yielded a total of 133,900,261 reads, revealing 7796 differentially expressed genes (DEGs). We constructed a gene regulatory network with 59 hub genes, identified 6783 transcription factors and uncovered 88,424 putative markers, including 17,236 simple‐sequence repeats (SSRs), 10,099 single‐nucleotide polymorphisms (SNPs) and 78,332 indels. Notably, the majority of DEGs were upregulated at 24 hpi in the resistant genotype, encompassing diverse functional categories such as pathogenesis‐related genes, defence‐related (R) genes, genes involved in plant–fungus interactions, oxidation–reduction‐related genes, transport, metabolism and proteolysis genes, along with transcription factors (FAR1, B3, GATA, NAC, WRKY, MYBC1 and bHLH), secondary metabolic pathway‐related genes and photosynthesis‐related genes. The up‐regulation of WRKY transcripts, associated with the activation of the jasmonic acid defence signalling pathway, potentially induced systemic acquired resistance (SAR). Conversely, these DEGs exhibited down‐regulation in the susceptible genotype. Furthermore, a total of 17,236 expressed sequence tag (EST)‐SSRs were identified from the unigenes, holding significant potential for advancing plant breeding through marker‐assisted methods, facilitating quantitative trait locus (QTL) mapping and evaluating genetic diversity among genotypes. This study's approach contributes to a more profound understanding of the molecular‐level defence mechanisms involved in the interaction between groundnuts and S. rolfsii. [ABSTRACT FROM AUTHOR]