<jats:title>Abstract</jats:title><jats:p>Symbiotic N<jats:sub>2</jats:sub>-fixing microorganisms have a crucial role in the assimilation of nitrogen by eukaryotes in nitrogen-limited environments<jats:sup>1–3</jats:sup>. Particularly among land plants, N<jats:sub>2</jats:sub>-fixing symbionts occur in a variety of distantly related plant lineages and often involve an intimate association between host and symbiont<jats:sup>2,4</jats:sup>. Descriptions of such intimate symbioses are lacking for seagrasses, which evolved around 100 million years ago from terrestrial flowering plants that migrated back to the sea<jats:sup>5</jats:sup>. Here we describe an N<jats:sub>2</jats:sub>-fixing symbiont, ‘<jats:italic>Candidatus</jats:italic> Celerinatantimonas neptuna’, that lives inside seagrass root tissue, where it provides ammonia and amino acids to its host in exchange for sugars. As such, this symbiosis is reminiscent of terrestrial N<jats:sub>2</jats:sub>-fixing plant symbioses. The symbiosis between <jats:italic>Ca</jats:italic>. C. neptuna and its host <jats:italic>Posidonia oceanica</jats:italic> enables highly productive seagrass meadows to thrive in the nitrogen-limited Mediterranean Sea. Relatives of <jats:italic>Ca</jats:italic>. C. neptuna occur worldwide in coastal ecosystems, in which they may form similar symbioses with other seagrasses and saltmarsh plants. Just like N<jats:sub>2</jats:sub>-fixing microorganisms might have aided the colonization of nitrogen-poor soils by early land plants<jats:sup>6</jats:sup>, the ancestors of <jats:italic>Ca</jats:italic>. C. neptuna and its relatives probably enabled flowering plants to invade nitrogen-poor marine habitats, where they formed extremely efficient blue carbon ecosystems<jats:sup>7</jats:sup>.</jats:p>