Valentino Rossi qualified second for Yamaha, just 0.055 seconds behind his countryman, with Honda's Dani Pedrosa completing the front row of the grid, 0.253 behind Dovizioso.
Spaniard Marquez was just 0.020 second slower than team mate Pedrosa, as he edged out former two-time world champion Jorge Lorenzo on his Yamaha.
The 21-year-old champion has 292 points to Pedrosa's 217, with Rossi on 214, and will retain the title should he maintain the 75-point gap at the head of the standings with three races remaining after this one.
Dovizioso's pole record timing at the Motegi circuit of one minute 44.502 seconds earned his team a first pole position since Casey Stoner at Valencia four years ago.
(Writing by Sudipto Ganguly; Editing by John O'Brien)
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