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<i>Fatty Acid Desaturase 2</i> (<i>FAD2</i>) controls the conversion of oleic acids into linoleic acids. Mutations in <i>FAD2</i> not only increase the high-oleic content, but also repress the leaf growth. However, the mechanism by which <i>FAD2</i> regulates the growth pathway has not been elucidated in peanut leaves with single-cell resolution. In this study, we isolated <i>fad2</i> mutant leaf protoplast cells to perform single-cell RNA sequencing. Approximately 24,988 individual cells with 10,249 expressed genes were classified into five major cell types. A comparative analysis of 3495 differentially expressed genes (DEGs) in distinct cell types demonstrated that <i>fad2</i> inhibited the expression of the cytokinin synthesis gene <i>LOG</i> in vascular cells, thereby repressing leaf growth. Further, pseudo-time trajectory analysis indicated that <i>fad2</i> repressed leaf cell differentiation, and cell-cycle evidence displayed that <i>fad2</i> perturbed the normal cell cycle to induce the majority of cells to drop into the S phase. Additionally, important transcription factors were filtered from the DEG profiles that connected the network involved in high-oleic acid accumulation (<i>WRKY6</i>), activated the hormone pathway (<i>WRKY23</i>, <i>ERF109</i>), and potentially regulated leaf growth (<i>ERF6</i>, <i>MYB102</i>, <i>WRKY30</i>). Collectively, our study describes different gene atlases in high-oleic and normal peanut seedling leaves, providing novel biological insights to elucidate the molecular mechanism of the high-oleic peanut-associated agronomic trait at the single-cell level.