Increasingly severe storm surge events may harm marine plants such as seagrasses by reducing salinities beyond species’ tolerances. For terrestrial and aquatic plants, recent studies show that belowground microbes associated with roots and sediments influence plant responses to environmental stress. However, how belowground microbes affect plant response to salinity stress is unknown. Using a fully factorial mesocosm aquaria experiment, we manipulated root and sediment microbes across salinity treatments (~33, 15, 3 ppt; over 10 days) to test whether microbial assemblages can mediate salinity stress in the seagrass Zostera muelleri. Low salinity stress was associated with reduced leaf length and width, and lower above and belowground biomass in seagrass. Plants with intact root microbes had reduced leaf necrosis at ambient and medium salinities, suggesting that root microbes provide a beneficial effect. Contrastingly, disrupting sediment microbes improved seagrass performance at ambient and moderately reduced salinities, while intact sediment microbes suppressed growth. Seagrass performance declined under extreme low salinity stress regardless of root or sediment treatment. Differences in belowground microbial communities were associated with salinity treatments and were consistent with experimental results. Together, these findings indicate that belowground microbial assemblages reflect seagrass health, opening new avenues for seagrass monitoring and management.