Arctic marine bacteria experience seasonal changes in temperature, salinity, light, and sea ice cover. Time-series and metagenomic studies have identified spatiotemporal patterns in Arctic microbial communities, but a lack of complete genomes has limited efforts to identify the extent of genomic diversity in Arctic populations. We cultured and sequenced the complete genomes of 34 Arctic marine bacteria to identify patterns of gene gain, loss, and rearrangement that structure genomes and underlie adaptations to Arctic conditions. We found that the most abundant lineage in the Arctic (SAR11) is comprised of diverse species and subspecies, each encoding 50-150 unique genes. Half of the 16 SAR11 genomes harbor a genomic island with the potential to enhance survival in the Arctic by utilizing the osmoprotectant and potential methyl donor glycine betaine. We also cultured and sequenced four species representing an uncultured family of <i>Pseudomonadales</i>, four subspecies of <i>Pseudothioglobus</i> (SUP05), a genus of high GC <i>Puniceispirillales</i> (SAR116), and a family of low GC SAR116. Time-series 16S rRNA amplicon data indicate that this culture collection represents up to 60% of the marine bacterial community in Arctic waters. Their genomes provide insights into the evolutionary processes that underlie bacterial diversity and adaptation to Arctic waters.IMPORTANCEGenetic diversity has limited efforts to assemble and compare whole genomes from natural populations of marine bacteria. We developed a cultivation-based population genomics approach to culture and sequence the complete genomes of bacteria from the Arctic Ocean. Cultures and closed genomes obtained in this study represent previously uncultured families, genera, and species from the most abundant lineages of bacteria in the Arctic. We report patterns of gene gain, loss, rearrangement, and adaptation in the dominant lineage (SAR11), as well as the size, composition, and structure of genomes from several other groups of marine bacteria. This work demonstrates the potential for cultivation-based high-throughput genomics to enhance understanding of the processes underlying genomic diversity and adaptation.