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On the annual and interannual scales, lake microbial communities are known to be heavily influenced by environmental conditions both in the lake and in its terrestrial surroundings. How-ever, the influence of landscape setting and environmental change on shaping these communities over a longer (millennial) timescale is rarely studied. Here, we applied an 18S metabarcoding approach to DNA preserved in Holocene sediment records from two pairs of co‐located Swedish mountain lakes. Our data revealed that the microbial eukaryotic communities were strongly influenced by catchment characteristics rather than location. More precisely, the microbial communities from the two bedrock lakes were largely dominated by unclassified Alveolata, while the peatland lakes showed a more diverse microbial community, with Ciliophora, Chlorophyta and Chytrids among the more predominant groups. Furthermore, for the two bedrock‐dominated lakes—where the oldest DNA samples are dated to only a few hundred years after the lake formation—certain Alveolata, Chlorophytes, Stramenopiles and Rhizaria taxa were found prevalent throughout all the sediment profiles. Our work highlights the importance of species sorting due to landscape setting and the persistence of microbial eukaryotic diversity over millennial timescales in shaping modern lake microbial communities.