The factors and processes that shape microbial genomes and determine the success of microbes in different environments have long attracted scientific interest. Here, leveraging 2855 metagenome-assembled genomes (MAGs) sampled by the Vanishing Glacier Projectfrom glacier-fed streams (GFSs), we shed light on the genomic architecture of the benthic microbiome in these harsh ecosystems — now vanishing because of climate change. Owing to glacial influence, the GFS benthic habitat is unstable, notoriously cold and ultra-oligotrophic. Along gradients of glacial influence and concomitant variation in benthic algal biomass across 149 GFSs draining Earth’s major mountain ranges, we show how genomes of GFS bacteria vary in terms of size, coding density, gene redundancy, and translational machinery. We develop a novel, phylogeny-rooted analytical framework that allows pinpointing the phylogenetic depth at which patterns in genomic trends occur. These analyses reveal both deep- and shallow- rooting phylogenetic patterns in genomic features associated with key GFS taxa and functional potential relevant to live in these ecosystems. Additionally, we highlight the role of several clades of Gammaproteobacteria in shaping community-level genomic architecture. Our work shows how genome architecture is shaped by selective environmental constraints in an extreme environment. These insights are important as they reveal putatively important adaptations to the GFS environment which is now changing at rapid pace due to climate change.