Marinimicrobia are widespread from the marine surface to the hadal zone. Major clades of Marinimicrobia have evolved to different ecotypes along with energy gradients, but their genomes in deeper waters and sediments have rarely been studied. Here we obtained 11 Marinimicrobia draft genomes from the water column in the full-ocean depth and the hadal sediments in the Mariana Trench. All the predicted genomic capabilities of the metagenome-assembled genomes (MAGs) are indicative of heterotrophic lifestyle. The MAGs from the hadal depths are distinct from those from the mesopelagic and bathypelagic depths by enrichment of the genes involved in amino acids metabolism and mismatch repair. Compared with the MAGs from waters, those from the sediments were dramatically expanded by acquiring the genes responsible for chemotaxis, mobility and the two-component systems. Marinimicrobia were apparently differentiated in the environments with different depths, organic matters and electronic acceptors. Our results also posit a potential evolutionary relationship between the species inhabiting the waters and sediments, indicating the occurrence of allopatric speciation in Marinimicrobia.