The ascorbate-glutathione (AsA-GSH) cycle plays a critical role in scavenging hydrogen peroxide in plants and contributes significantly to plant stress tolerance. This study examines the cycle’s response in Zostera marina seedlings to warming, specifically under conditions of abnormal sea temperature increase. Three temperature gradients were established: 18°C (control group), 23°C (high-temperature group), and 28°C (abnormally high-temperature group). Results after 7 days of exposure to mild high temperature (23°C) showed decreased MDA content in the HT group, increased AsA/DHA ratio, and enhanced activity of enzymes related to the AsA-GSH cycle. However, exposure to extreme high temperatures resulted in increased oxidative damage and redox imbalance in the AHT group. Initially, enzymes associated with the AsA-GSH cycle, such as APX, MDHAR, GPX, and γ-ECS, increased but significantly decreased later under stress. In contrast, DHAR and GaILDH levels significantly rose on the seventh day. Transcriptome analysis revealed upregulation of APX, MDHAR, DHAR, GR, and γ-ECS genes in the HT group, with a decline in other enzyme gene expressions by the seventh day, except for APX. Under extreme high temperatures, APX expression was downregulated early in the stress period, while DHAR was upregulated, indicating Z. marina seedlings can mitigate oxidative damage under short-term high temperatures by activating the AsA-GSH cycle. Conversely, extreme high temperatures may inhibit this cycle, disrupt redox balance, and adversely affect Z. marina seedling establishment, potentially leading to their demise.