Abstract78 million tons of residual seagrass deposits accumulate annually on shorelines worldwide. These represent an untapped feedstock for fermentative single‐cell oil production, targeted at biofuel and oleochemical generation, without affecting the sensitive marine environment or compromising food security. Seven beach‐cast samples of seagrass (related to Z. marina, Z. noltii, S. filiforme, P. australis, P. oceanic, and T. testudinum) were collected from marine ecosystems around the world. A combination of 18S rRNA phylogenetic, structural, and comprehensive biomass analyses of seagrass leaves were applied. The carbohydrate content ranged from 73 to 81 % (w/dwbiomass). Single‐step enzymatic hydrolysis was developed to efficiently release the monomeric sugars contained in seagrasses biomass without any pretreatment. P. oceanica hydrolysate allowed for higher lipid yields (6.8 g L−1) compared to the synthetic minimal medium (5.1 g L−1) in shake flasks, and was subsequently utilized as the sole fermentation medium for oleaginous yeast T. oleaginosus at a technical scale using a fed‐batch bioreactor, which provided 24.5 g L−1 lipids (0.35 g L−1 h−1). Moreover, the sugar/lipid conversion ratio was 0.41 (w/w). Cumulative data indicates that by exploiting only half of the global beach‐cast seagrass, approximately 4 million tons of microbial oils could be generated.