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Abstract Cycloalkanes are abundant and toxic compounds in subsurface petroleum reservoirs and their fate is important to ecosystems impacted by natural oil seeps and spills. This study focuses on the microbial metabolism of methylcyclohexane (MCH) and methylcyclopentane (MCP) in the deep Gulf of Mexico. MCH and MCP are often abundant cycloalkanes observed in petroleum and will dissolve into the water column when introduced at the seafloor via a spill or natural seep. We conducted incubations with deep Gulf of Mexico (GOM) seawater amended with MCH and MCP at four stations. Within incubations with active respiration of MCH and MCP, we found that a novel genus of bacteria belonging to thePorticoccaceaefamily (Candidatus Reddybacter) dominated the microbial community. Using metagenome‐assembled genomes, we reconstructed the central metabolism ofCandidatus Reddybacter, identifying a novel clade of the particulate hydrocarbon monooxygenase (pmo) that may play a central role in MCH and MCP metabolism. Through comparative analysis of 174 genomes, we parsed the taxonomy of thePorticoccaceaefamily and found evidence suggesting the acquisition ofpmoand other genes related to the degradation of cyclic and branched hydrophobic compounds were likely key events in the ecology and evolution of this group of organisms.