Seagrass meadows are autotrophic ecosystems acting as carbon sinks, but they have also been shown to be sources of carbon dioxide (CO2) and methane (CH4). Seagrasses can be negatively affected by increasing seawater temperatures, but the effects of warming on CO2 and CH4 fluxes in seagrass meadows have not yet been reported. Here, we examine the effect of two disturbances on air–seawater fluxes of CO2 and CH4 in Red Sea Halophila stipulacea communities compared to adjacent unvegetated sediments using cavity ring-down spectroscopy. We first characterized CO2 and CH4 fluxes in vegetated and adjacent unvegetated sediments, and then experimentally examined their response, along with that of the carbon (C) isotopic signature of CO2 and CH4, to gradual warming from 25 ∘C (winter seawater temperature) to 37 ∘C, 2 ∘C above current maximum temperature. In addition, we assessed the response to prolonged darkness, thereby providing insights into the possible role of suppressing plant photosynthesis in supporting CO2 and CH4 fluxes. We detected 6-fold-higher CO2 fluxes in vegetated compared to bare sediments, as well as 10- to 100-fold-higher CH4 fluxes. Warming led to an increase in net CO2 and CH4 fluxes, reaching average fluxes of 10 422.18 ± 2570.12 µmol CO2 m−2 d−1 and 88.11±15.19 µmol CH4 m−2 d−1, while CO2 and CH4 fluxes decreased over time in sediments maintained at 25 ∘C. Prolonged darkness led to an increase in CO2 fluxes but a decrease in CH4 fluxes in vegetated sediments. These results add to previous research identifying Red Sea seagrass meadows as a significant source of CH4, while also indicating that sublethal warming may lead to increased emissions of greenhouse gases from seagrass meadows, providing a feedback mechanism that may contribute to further enhancing global warming.