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Developing new antibiotics is a critical area of research that grows as a result of the increasing problem of antibiotic resistance. Scientists search for new antibiotics by screening natural sources such as soil, plants, and marine environments. One of the iconic plants in the marine environment is the mangrove, which is a source of honeybee propolis. Propolis collected from the grey mangrove Avicennia marina on Tarout Island, the Eastern Province of Saudi Arabia, was used to evaluate antibacterial activities against three pathogenic bacteria: gram-negative Enterobacter cloacae (RCMB 001(1) ATCC^® 23355^TM), gram-positive methicillin-resistant Staphylococcus aureus (clinical isolate), and Streptococcus mutans Clark (RCMB 017(1) ATCC^® 25175^TM). The results indicate the effectiveness of the methanolic extract of such propolis. The chemical composition of this extract was analyzed using LC-MS, and four compounds were identified (alginic acid, carrageenan, fucoxanthin, cycloeudesmol). Their modes of action were evaluated against bacterial cell walls. Bacterial transpeptidase and transglycosylase on the surface are basic for cell divider amalgamation, and numerous antimicrobials have been created to target these compounds. Molecular docking was employed to predict the interactions of four compounds and S. aureus to predict interaction. Alginic acid was found to be the best interaction with a score of −7.44 Kcal/mol with distance ranges between 2.86 and 3.64 and RMSD refined below 2 Å. Carrageenan with −6.64 Kcal/mol and a distance of 3.05 and 2.87 came second. Then, fucoxanthin with −6.57 Kcal/mol and a distance of 1.4. Finally, cycloeudesmol with a score of −4.6 Kcal/mol and a distance of 2.87 showed the least activity. The first three compounds interacted effectively and could form very promising chemicals that could be used one day against pathogenic bacteria in the future. Full article