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Introduction Prostate cancer is an extremely variable and multifaceted malignancy and has significant contributor to morbidity and mortality in males. Current therapies frequently resulting in significant adverse consequences. Pumpkin seed oil (PSO) has antibacterial, antiviral, cytotoxic, and anticancer properties. Nevertheless, its hydrophobic characteristics restrict bioavailability, which might be enhanced using nanoemulsion based delivery system. In our previous study, the formulation and characterization of pumpkin seed oil nanoemulsion (PSO-NE) was investigated and observed that PSO-NE induces cytotoxicity in breast cancer cells (MCF-7 and MDA-MB-231). Nonetheless, a PSO-NE has not been studied in prostate cancer research, whether in vitro or in vivo . The primary aim of this work was to evaluate PSO-NE cytotoxic and apoptotic effects on prostate cancer cell lines (PC3 and LNCaP). Methods Cytotoxicity efficacy was assessed using MTT assay. Cellular uptake and nuclear morphology were evaluated through confocal microscopy. Mechanistic assays included apoptosis, proliferation, and cell cycle analysis were evaluated through flow cytometry. Differential gene expression was quantified by real-time PCR. Results In this study, PSO-NE exhibited dose-dependent cytotoxicity, demonstrating a markedly reduced IC 50 in comparison to free PSO and Doxorubicin after 24 h of exposure (p < 0.01) accompanied with reduced cytotoxicity towards non-cancerous cells (Vero). At IC 50 concentrations (PC3 = 90.22 μg/mL and LNCaP = 65.47 μg/mL), PSO-NE strongly induced nucleus morphological changes, reduced cell proliferation, increased phosphatidylserine exposure, and arrested the cell cycle at G0/ G1 phase (p < 0.001). The expression of genes (Bcl-2, STAT-3, and NF-kB), related to cell proliferation, was significantly downregulated (p < 0.001), whereas the expression of genes (p53, Bax, and caspase 3), associated with apoptosis, was significantly upregulated compared to the untreated cell lines (p < 0.001), indicating the activation of apoptotic gene expression. Discussion The enhanced cytotoxicity of PSO-NE against prostate cancer cells, together with its capacity to cause apoptosis and cell cycle arrest, highlights its potential as an effective anticancer agent.