Abstract <p>Obligate marine fungi associated with mangroves are a unique group that fulfils significant ecological functions in mangrove ecosystems. The present study aimed to assess the antimicrobial, antioxidant, and anticancer potentials of the marine fungus “<i>Swampomyces armeniacus</i>” isolated and characterized (on both morphological and molecular levels) from mangroves located in RAS Mohamed natural protectorate on the Red Sea coast; along with determining the metabolomics profiling of the candidate species. The antimicrobial capability was assessed via the agar well diffusion method against 6 strains (<i>Bacillus cereus, Staphylococcus aureus, Shigella sonnei, Pseudomonas aeruginosa, Candida albicans,</i> and <i>Aspergillus niger)</i> alongside determining the minimum inhibitory concentration (MIC) by two-fold microdilution method. The study findings indicated that <i>S. armeniacus</i> crude extract had antimicrobial activity against all test strains whereas the strongest effect was against <i>B. cereus</i> with MIC value 0.7 μg/ml. Moreover, the antioxidant potential was determined via DPPH which showed strong radical scavenging activity of 88.3% and IC50 = 20.4 μg/mL. Additionally, the extract exhibited significant anticancer activity against A549 lung cancer cells, with an IC50 value of 15.57 ± 0.27 µg/mL, while showing minimal toxicity toward normal Wi38 cells (IC50 = 37.71 ± 0.31 µg/mL). GC–MS investigation of <i>S. armeniacus</i> crude extract exhibiting antimicrobial, antioxidant, and anticancer related bioactive compounds such as (Di-tert-butylhydroquinone, 4-Aminocyclohexanecarboxylic acid) and various fatty acids namely (stearic acid, palmitic acid, Ethanedioic acid, and Butanedioic acid). These results highlight the biological activity of <i>S. armeniacus</i> and emphasizing its potential as a unique source of bioactive molecules for biotechnological and therapeutic applications.</p> Graphical Abstract <p></p>