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Abstract Lake Baikal is the deepest lake in the world. Its depth provides the only bathypelagic (> 1000 m deep) freshwater habitat on Earth and its oxic, ultra‐oligotrophic features make it a freshwater counterpart of the deep ocean. Here we have analyzed metagenomes from 1250 and 1350 m deep samples and built 231 metagenome‐assembled genomes (MAGs). We detected high fractions of Thaumarchaeota (ca. 20% of 16S rRNA reads) and members of the candidate phyla radiation (CPR) (3–4.5%). Among the MAGs, we obtained ammonia‐oxidizing archaea (AOA, Nitrosopumilaceae) and bacteria (AOB, Nitrosomonadaceae), and nitrite‐oxidizers (Nitrospirae) indicating very active nitrification. A new clade of freshwater SAR202 Chloroflexi and methanotrophs ( Methyloglobulus ) were also remarkably abundant, the latter reflecting a possible role of methane oxidation as well. Novel species of streamlined and cosmopolitan bacteria such as Ca. Fonsibacter or acI Actinobacteria were more abundant at the surface but also present in deep waters. Conversely, CPRs, Myxococcales, Chloroflexi, DPANN (Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanoarchaeota and Nanohaloarchaeota) archaea, or Gammaproteobacteria were found only in bathypelagic samples. We noted various important taxonomic and metabolic differences between deep aphotic region of Lake Baikal and marine waters of similar depth: Betaproteobacteriales, CPR, and DPANN superphylum were only found in bathypelagic Baikal, while Deltaproteobacteria, Gammaproteobacteria, or Alphaproteobacteria prevailed in oceanic samples. The genes mediating ammonia and methane oxidation, aromatic compound degradation, or alkane/methanesulfonate monooxygenases were detected in higher numbers in deep Baikal compared to their oceanic counterparts or its own surface. Overall, depth seems to be less relevant than salinity in configuring the microbial community.