Summary Spatial and temporal heterogeneity in flowering occur in many plant species with abiotic pollination and may confer fitness advantages through mechanisms such as predator satiation or pollination efficiency. Environmental factors such as light quality or quantity and temperature play an important role in inducing synchronization on wide geographic scales. On a smaller geographic scale, external factors such as resource availability and herbivory are theorized to trigger flowering, while genetic factors may also play an important role. In this study, we assessed the importance of ecological and genetic factors in shaping seascape‐level spatial heterogeneity in flowering of the seagrass Posidonia oceanica. By investigating spatially close sites (<20 km) with similar seascape configurations and depth, we assume that major environmental drivers (temperature and light) were equivalent. We assessed four ecological factors (productivity, leaf nitrogen and carbon content and herbivory) and three genetic factors (heterozygosity, relatedness and clonality) to assess three hypotheses for synchronized flowering in P. oceanica: (i) clone synchronization (internal clock hypothesis), (ii) variation in nutrient availability, potentially caused by spatial heterogeneity in herbivory rates or nutrient translocation via clonal integration (resource budget hypothesis) or (iii) kin selection and sibling synchronization. Internal relatedness and heterozygosity had a significant positive effect on the abundance of flowers. Moreover, productivity and genotypic richness (clonality) were negatively associated with flower density, although at a lower level of significance. In addition, we found that clones were almost exclusively shared among mass‐flowering patches and patches without mass‐flowering, respectively. Synthesis. The results shed new light on seagrass flowering patterns and on the mechanisms of flower synchronization at the patch level within a wider spatial scale. We found support for the kin selection hypothesis and indirect evidence for the resource budget hypothesis. Thus, a combination of mainly genetic but also ecological factors causes the observed heterogeneous flowering patterns in Posidonia oceanica seascapes. In addition, we found a strong positive relationship between the number of flowers and heterozygosity, adding evidence to the controversial association between heterozygosity and fitness when a limited number of loci are used. To our knowledge, this study is the first to link both ecological and genetic factors with flower abundance in a species with a presumed masting strategy.