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Numerous studies have accumulatively discovered mitochondrial genome (mtDNA) diversity in the natural populations of the same species, and some of the mtDNA variations may be selected by the host's environment. However, it remains unclear about the molecular mechanisms by which this long-term coexistence of mtDNA variations in the same species affects the metabolism and evolution of the host. By comparing two mitochondrial genomes of cultured population of Hermetia illucens, our study reveals that the mtDNAs of both strains (Ref-strain and Sub-strain) have great structural divergences, and mitochondria of the Sub-strain may be functionally defective, which is consistent with the observed lower body weights and higher oxidative stress levels in the midgut of Sub-strain. Moreover, the differentially expressed genes and differential metabolites between the midguts of both strains were related to the mitochondrial functions including oxidative stress, antioxidant and electron transport chain. Interesting, the midgut microbial compositions differed significantly in both strains. Additionally, 25 of 310 the potentially positively selected genes were related to mitochondrial function. Combination of these multidimensional investigations of both strains helped to reveal how the host insects adapt to mtDNA variations through cyto-nuclear interactions. This study can provide new evidence for understanding the nuclear response to the mitochondria dysfunction in insects, and its role in differentiation of the natural populations and even in the process of speciation. [ABSTRACT FROM AUTHOR]