Ahmad Wali Karzai, a leading power broker in the country's south, was shot dead at his home in a blow to Nato's battle against the Taliban in the area.
He was shot twice by his long-time head of security, Sardar Mohammed, who was himself killed almost immediately.
The Taliban said they carried out the attack, calling it one of their top achievements in 10 years of war.
But Khaled Pashtun, a Kandahar province politician, was sceptical about the Taliban claims, saying the Islamist group had claimed responsibility for many attacks in the past without much evidence of their involvement.
The White House condemned the assassination "in the strongest possible terms".
Sardar Mohammed's motives remain unclear, but the killing will raise questions about securing Afghanistan's top officials.
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