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Abstract Interactions between phytoplankton and bacteria play critical roles in shaping marine ecosystems. However, the intricate relationships within these communities—particularly in rapidly changing polar environments—remain poorly understood. We use targeted methods to directly characterize the microbiomes of individual colonies ofPhaeocystis antarctica, a keystone phytoplankton species in the Southern Ocean, and showed that colony microbiomes were consistent across individual colonies collected 108 nautical miles apart. These results suggest that hosting specific colony microbiomes is a shared trait across colony‐formingPhaeocystisspecies, with different species hosting colony microbiomes suited to their respective environments. The bacterial orders Alteromonadales, Oceanospirillales, and Sphingomonadales dominated the microbiomes of all field‐collectedP. antarcticacolonies. The relative abundances of bacterial taxa comprising the majority of field‐collected colony microbiomes—for example,Paraglaciecolasp. (Alteromonadales) and Nitrincolaceae (Oceanospirillales)—correlated withPhaeocystisabundance in surface waters, highlighting their potential roles in bloom dynamics and carbon cycling. After a year of laboratory culture, we observed a reduction in colony microbiome diversity, and Caulobacterales, Cellvibrionales, and Rhodobacterales dominated the cultured colony microbiomes. Notably, abundant genera in field‐collected colony microbiomes that were lost in culture were psychrophiles. The shift in microbiome structure emphasizes the importance of field‐based studies to capture the complexity of microbial interactions, especially for species from polar environments that are difficult to replicate in laboratory conditions. This research provides valuable insights into the ecological significance of prokaryotic interactions with a key phytoplankton species and underscores the necessity of considering these dynamics in the context of climate‐driven shifts in marine ecosystems.