Marine Nitrososphaerota are among the most abundant archaea in the ocean and play critical roles in global biogeochemical cycles. While the ecology of ammonia-oxidizing archaea (AOA) has been extensively studied, much less is known about heterotrophic marine Nitrososphaerota (HMN), the second most abundant lineage within this phylum. Previous observations suggested a consistent co-occurrence between HMN and marine AOA (MAOA), raising questions about the ecological and evolutionary mechanisms underlying their association. To address this knowledge gap, we integrated analyses of 104 HMN genomes, global metagenomic and metatranscriptomic datasets from the South China Sea, Western Pacific, Tara Oceans, and Malaspina expeditions, together with catalyzed reporter deposition fluorescence in situ hybridization (CARD-FISH). Global recruitment analyses revealed a strong positive correlation between HMN and MAOA abundances and demonstrated ecotype-specific associations between shallow and deep-water lineages. Comparative genomics revealed the absence of most B vitamin biosynthesis pathways, incomplete citrate cycle and glycolysis, and a requirement for exogenous amino acids in HMN, suggesting potential metabolic coupling with co-occurring MAOA. CARD-FISH imaging further revealed that approximately 83.8% of HMN cells were physically associated with MAOA cells in situ, supporting a close cellular relationship in the marine environment. Evolutionary analyses indicated that HMN and AOA originated during similar geological periods following the rise of atmospheric oxygen. Evolutionary analyses revealed extensive loss of vitamin and cofactor biosynthesis genes in HMN, contrasting with the acquisition of these functions in AOA, resulting in complementary metabolic capabilities between the two lineages. Horizontal gene transfer analyses indicated that HMN acquired key genes involved in heterotrophic metabolism from bacteria, while potential gene exchange with co-occurring AOA suggests a long-term evolutionary association between the two lineages. Together, these findings reveal a previously unrecognized ecological association between heterotrophic and ammonia-oxidizing marine Nitrososphaerota. This association links heterotrophic and chemolithoautotrophic processes in the deep ocean and provides new insights into archaeal interactions, evolutionary adaptation, and carbon and nitrogen cycling in marine ecosystems.