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Premise: There is growing recognition that intraspecific genetic variation in plants can influence associated soil microbial communities, but the functional bridges linking plant genotype with microbial community structure are not well understood. This deficit is due in part to a prevailing focus on characterizing relationships between microbial communities and functional trait variation among plant species or across plant communities, rather than within a single species. Methods: We examined whether and how spatiotemporal variation in salt marsh rhizosphere microbial communities reflect plant provenance (genotypic variation) and associated trait variation within an ecosystem engineer, Spartina alterniflora. We planted S. alterniflora from four genetically distinct source populations in replicate sets of experimental plots across a shoreline in southeastern Louisiana, USA. After 2 years, we measured functional plant traits and profiled microbial communities. Results: Bacterial and fungal α‐diversity and richness were significantly higher in winter than in summer and corresponded to plant trait variation associated with provenance. Notably, 20% of the variation in fungal community composition was explained by trait differences while bacterial community structure did not reflect plant provenance or trait variation. However, evidence was found suggesting that bacterial communities are indirectly shaped by the influence of plant provenance on soil physicochemical properties. Conclusions: This study illustrates that intraspecific genetic and corresponding trait variation in an ecosystem engineer can shape rhizosphere microbial communities, with fungal communities being more responsive than bacteria to the influence of plant provenance and associated trait variation. Our results highlight the potential relevance of plant intraspecific variation in plant–microbe–soil feedbacks shaping naturally depauperate ecosystems like salt marshes. [ABSTRACT FROM AUTHOR]