Background <p>Seed endophytes are the earliest microbial companions of plants. They play a beneficial role in seed germination, seedling development, and plant growth. Endophytes help plants to adapt to changing environments; however, their role in the aspect of toxic metal-polluted environments is poorly known. We investigated the impact of metal toxicity on the structure of seed-associated microbiota in <i>Arabidopsis arenosa</i> and explored the role of these microbes in host plant adaptation to metal-rich, post-mining environments.</p> Results <p>Toxic metals markedly altered the alpha and beta diversity of bacterial seed endophytes, whereas fungal endophyte diversity was largely unaffected. Similar patterns were observed in a vertical transmission experiment, indicating that metal exposure can influence seed-associated microbiota across generations. To explore the functional relevance of these changes, we assembled synthetic microbial communities from culturable bacterial and fungal isolates recovered from seeds of plants originating from non-metalliferous and metalliferous sites. A synthetic community composed of isolates from non-metalliferous populations enhanced plant growth under metal stress, whereas the community assembled from metalliferous populations showed no growth-promoting effect. Crude seed extracts also did not reproduce the growth-promoting effect of the defined synthetic community. Further fractionation indicated that the beneficial effect was mainly associated with the fungal component, while bacterial fractions did not enhance plant growth under the tested metal-stress conditions. Fungal isolates from non-metalliferous populations promoted plant biomass under metal stress, whereas this effect was not observed for isolates from metalliferous populations under the tested conditions.</p> Conclusions <p>Long-term exposure to toxic metals exerts strong selective pressure on seed-associated microbiota, markedly reducing bacterial diversity and reshaping community composition while leaving fungal diversity largely unaffected. Metal toxicity causes losses in the abundance of bacteria. High metal tolerance of these microorganisms indicates rather that metal exposure affects the interaction between the microbe and its host and the ability of the microbe to be retained in the seeds. Fungal endophytes from metal-free populations proved more effective in promoting plant growth under metal stress than those from metalliferous populations, suggesting that intrinsic strain-level traits, rather than prior environmental adaptation, are key to enhancing host tolerance. This challenges the assumption that endophytes from contaminated sites are inherently better suited for phytoremediation and highlights the potential of “naive” microbial sources. Together, these results expand our understanding of vertical transmission, microbial adaptation, and host–microbe interactions under heavy metal stress, and underscore the value of broadening the search for effective endophytes beyond contaminated habitats.</p>