Water column hypoxia, low partial pressure of oxygen (pO₂), and hydrogen sulfide (H₂S) intrusion, a phytotoxin, are factors linked to global seagrass decline. While many lab experiments have examined these relationships, field studies are needed to elucidate complex drivers of internal pO₂ in situ. Herein, we examined plant pO₂ and H₂S dynamics using microsensors in a dominant tropical seagrass Thalassia testudinum in Florida Bay, a subtropical estuary with recurrent seagrass die-off events. Based on 12 field deployments (48–72 h) across seasons, we show that T. testudinum has a high capacity for daytime leaf oxidation (42–53 kPa) that sustains oxic conditions in its tissues and supersaturates the water column with O₂ (> 21 kPa). Although internal daytime O₂ is rapidly consumed near sunset, daytime seagrass O₂ production leads to supersaturation in the water column beyond sunset. This is an important feedback mechanism as high water column pO₂ at night buffers against internal leaf hypoxia via diffusion. Even with high daytime irradiance, however, shoot meristems went anoxic/hypoxic (0.6 kPa) at night, indicating high plant and ecosystem O₂ consumption. Hydrogen sulfide was only detected in the meristem when water column pO₂ was close to anoxia (< 1 kPa) coincident with maximum water column temperatures (33 °C), an occurrence likely to increase with global warming. Our results support the hypothesis that meristem H₂S intrusion in Florida Bay, and likely globally, is primarily driven by insufficient internal plant oxidation by the water column at night, even when high irradiance sustains supersaturation of tissue O₂ during the day.