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Genetic diversity can modulate a population's response to a changing environment and plays a critical role in its ecological function. While multiple processes act to maintain genetic diversity, sexual reproduction remains the primary driving force. Eelgrass (Zostera marina) is an important habitat‐forming species found in temperate coastal ecosystems across the globe. Recent increases in sea surface temperatures have resulted in shifts to a mixed‐annual life‐history strategy (i.e., displaying characteristics of both annual and perennial meadows) at its southern edge‐of‐range. Given that mating systems are intimately linked to standing levels of genetic variation, understanding the scope of sexual reproduction can illuminate the processes that shape genetic diversity. To characterize edge‐of‐range eelgrass mating systems, developing seeds on flowering Z. marina shoots were genotyped from three meadows in Topsail, North Carolina. In all meadows, levels of multiple mating were high, with shoots pollinated by an average of eight sires (range: 3–16). The number of fertilized seeds (i.e., reproductive success) varied significantly across sires (range: 1–25) and was positively correlated with both individual heterozygosity and self‐fertilization. Outcrossing rates were high (approx. 70%) and varied across spathes. No clones were detected, and kinship among sampled flowering shoots was low, supporting observed patterns of reproductive output. Given the role that genetic diversity plays in enhancing resistance to and resilience from ecological disturbance, disentangling the links between life history, sexual reproduction, and genetic variation will aid in informing the management and conservation of this key foundation species. This study provides a thorough description of fine‐scale patterns in Zostera marina's mating system at the species' southern edge‐of‐range, an area where eelgrass experiences frequent summer heat stress. Sampled populations displayed a reliance on sexual recruitment, and male quality was linked to reproductive success. Our findings serve as stepping stones to further understand the evolutionary processes underpinning seagrass genetic composition and life history, which is essential for informed conservation and management. [ABSTRACT FROM AUTHOR]