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<i>Cordyceps militaris</i> has been used for treating various diseases, as well as maintaining good overall health. The antibacterial properties of the <i>C. militaris</i> fruiting body and substrate, cultured in Chiang Mai (sample A and B) and Chiang Rai (sample C), Thailand, were investigated in this study. The aqueous and ethanolic extracts of <i>C. militaris</i> exhibited antibacterial activities against <i>Staphylococcus aureus</i>, <i>Pseudomonas aeruginosa</i>, <i>Cutibacterium acnes</i> and methicillin-resistant <i>S. aureus</i> (MRSA) with the MIC/MBC ranging from 3.91 to 31.25 mg/mL. The ethanolic extracts of the fruiting body and substrate from sample B also inhibited all bacterial growth within 2–4 h of treatment. Furthermore, ethanolic extract from sample B showed the highest cordycepin content of 57.42 mg/g extract, whereas the highest adenosine content, 3.78 mg/g extract, was observed in the ethanolic extract from the fruiting body of sample A by HPLC. The ethanolic extracts from sample A also demonstrated the highest antioxidant activity and flavonoid content by 9.50 mg GAE/g extract and 10.59 mg QAE/g extract, respectively. However, the highest phenolic content of 49.04 mg GAE/g extract was found in the aqueous extract of sample A. In addition, the ethanolic extract of sample A at 2 and 4 mg/mL could significantly down-regulate the <i>mecA</i> gene expression in MRSA. Our findings reported the potential of <i>C. militaris</i> extract as a new substance for the treatment of skin pathogenic bacteria infections and an antioxidant agent.