Red dragon fruit is gaining popularity globally due to its nutritional value and bioactive components. The study aimed to assess the phytochemical, nutritional composition, antioxidant, antibacterial, and cytotoxic properties of extracts from the South Chinese red dragon fruit peel, flesh, and seeds. Extract fractions with increasing polarity (ethyl acetate<acetone<ethanol<methanol) were prepared. Significant amounts of nutritional components (minerals, protein, sugars, vitamins, fatty acids) were found in all parts of the fruit. The ethanol (ET) and methanol (MT) fractions of all the extracts exhibited significant antioxidant activity, with EC₅₀ values ranging from 3.25–8.30 μg/mL. The flesh MT and ET extract fractions demonstrated substantial inhibitory effects, with MIC₅₀ ranging 73.62–98.85 μg/mL, against several multidrug-resistant bacteria. Cytotoxicity assays revealed no adverse effects of the crude extract fractions on human keratinocytes (HaCaT) cells (from adult human skin). Liquid chromatography with tandem mass spectrometry (LC-MS/MS) and gas chromatography-tandem mass spectrometry (GC-MS/MS) analyses unveiled a wide array of compounds with known and unknown antibacterial and antioxidant activities. Thereafter, pharmacological property screening and molecular docking were performed. The results identified four active compounds, baicalein, quercetin, morin, and isorhamnetin, which demonstrated strong binding affinity with the selected target proteins and complied with most of the pharmacological parameters. In conclusion, this study provides essential information on the key nutrients present in the peel, flesh, and seeds of the red dragon fruit from Southern-China. Furthermore, it highlights the potential of ET and MT fractions, which contain compounds with promising antibacterial properties.