Kay's book was chosen from 91 submissions to win the Â£30,000 prize.
It is the first time the public have voted for a winner but the novel was also unanimously selected by the award's judging panel.
Leila Aboulela, Stewart Conn and Sue Peebles came in as runners-up, winning Â£5,000 each.
Kay was born in Edinburgh to a Scottish nurse and a Nigerian student, then adopted at birth by a white couple from Glasgow.
Red Dust Road follows the author in her search to find her birth parents.
She said: "I happened to write the book, but it feels like my whole family is the winner. The book doesn't just belong to me.
"And now it seems like it has a whole life of its own in the heart-warming and unexpected way that readers have been finding connections to their own life in it."
The prize has been won by James Kelman and Edwin Morgan in previous years.
Andrew Dixon, chief executive of Creative Scotland, said: "With more than 40 literature and book festivals from the Borders to Ullapool, Scotland's writers continue to raise Scotland's cultural profile to an international audience.
"Jackie Kay is one of Scotland's national treasures."
Scottish author Jackie Kay has won the 2011 Scottish Mortgage Investment Trust Book of the Year for her autobiographical novel Red Dust Road.