The competitor was riding the first leg of the race from Alice Springs to Aputula/Finke on Sunday when the crash occurred after midday, Northern Territory Police said.
Police provided first aid until paramedics arrived but the rider died at the scene.
A crime scene has been declared and crash detectives are preparing a report for the coroner.
Finke Desert Race NT Police Commander Michael Budge said the incident was a tragedy for all involved.
"Our thoughts are with the rider's family, friends and all involved with the event at this difficult time," he said.
Race authorities have extended their deepest sympathies and condolences to the rider's family and friends and are providing ongoing support at both ends of the event route.
The renowned desert motor race, which is marking its 50th year, features dirt bikes and buggies speeding across a 450km red-dirt track in Central Australia.
The fatality is not the first to occur at the event.
In 2021, 60-year-old Canberra retiree Nigel Harris died when a competing vehicle veered into a crowd of spectators after its suspension failed.
His death led to the introduction of a 30-metre buffer zone between spectators and the track.
A Queensland motorcycle rider died in 2008 after he crashed into a tree while racing in the event.
The King's birthday weekend Finke Desert Race has attracted more than 800 competitors including men, women and junior riders - a more than 60 per cent increase on 2025.
The main race is from Alice Springs to Aputula/Finke and back over two days, with many thousands of spectators lining the dusty trail to see who becomes "King of the Desert".Â
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