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Motility regulation plays a key role in prokaryotic responses to environmental stimuli. Here, we used a motility screen and selection to isolate hypermotile Haloferax volcanii mutants from a transposon insertion library. Whole genome sequencing revealed that hypermotile mutants were predominantly affected in two genes that encode HVO_1357 and HVO_2248. Alterations of these genes comprised not only transposon insertions but also secondary genome alterations. HVO_1357 contains a domain that was previously identified in the regulation of bacteriorhodopsin transcription, as well as other domains frequently found in two-component regulatory systems. The genes adjacent to hvo_1357 encode a sensor box histidine kinase and a response regulator, key players of a two-component regulatory system. None of the homologues of HVO_2248 have been characterized, nor does it contain any of the assigned InterPro domains. However, in a significant number of Haloferax species, the adjacent gene codes for a chemotaxis receptor/transducer. Our results provide a foundation for characterizing the root causes underlying Hfx. volcanii hypermotility.