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Simple Summary: Anopheles mosquitoes are the only vectors of human malaria, a deadly disease causing over 500,000 deaths annually, mainly in sub-Saharan Africa. Less than 10% of the roughly 500 Anopheles species are malaria vectors. Although malaria has been eliminated in Europe, Anopheles mosquito species remain a focus of research due to their potential to transmit malaria and other infectious diseases. Understanding the evolution of vectorial capacity can be enhanced by knowledge of the speciation and adaptation of malaria mosquitoes. Chromosomal inversions, such as large-scale genomic rearrangements, are believed to play a role in the ability of mosquitoes to diversify and adapt to human-created environments. However, genome mapping and the characterization of chromosomal inversions have only been conducted on a small fraction of malaria mosquito species. In this study, we mapped and characterized inversions that differentiate the European mosquito Anopheles atroparvus and the Eurasian mosquito An. messeae. Two small genomic blocks underwent a change in position and orientation on the X chromosome between the two species. The rearranged chromosomal regions are enriched with genes that play roles in regulating the immune system and mating behavior. These findings offer insight into the underlying molecular mechanisms behind the differences in susceptibility to infection and behavior between An. atroparvus and An. messeae. The Maculipennis subgroup of malaria mosquitoes includes both dominant malaria vectors and non-vectors in Eurasia. Understanding the genetic factors, particularly chromosomal inversions, that differentiate Anopheles species can provide valuable insights for vector control strategies. Although autosomal inversions between the species in this subgroup have been characterized based on the chromosomal banding patterns, the number and positions of rearrangements in the X chromosome remain unclear due to the divergent banding patterns. Here, we identified two large X chromosomal inversions, approximately 13 Mb and 10 Mb in size, using fluorescence in situ hybridization. The inversion breakpoint regions were mapped by hybridizing 53 gene markers with polytene chromosomes of An. messeae. The DNA probes were designed based on gene sequences from the annotated An. atroparvus genome. The two nested inversions resulted in five syntenic blocks. Only two small syntenic blocks, which encompass 181 annotated genes in the An. atroparvus genome, changed their position and orientation in the X chromosome. The analysis of the An. atroparvus genome revealed an enrichment of gene ontology terms associated with immune system and mating behavior in the rearranged syntenic blocks. Additionally, the enrichment of DNA transposons was found in sequences homologous to three of the four breakpoint regions. This study demonstrates the successful application of the physical genome mapping approach to identify rearrangements that differentiate species in insects with polytene chromosomes. [ABSTRACT FROM AUTHOR]