Jamaica won in 37.36secs with the United States second and Canada third after Great Britain were disqualified.
Britain lost their bronze after an appeal was lodged against their second changeover.
Bolt, who has now won the 100m, 200m and 4×100m World Championships triples on two occasions, joins American’s Michael Johnson in the history book on a record-equaling eight world titles overall, plus two silvers.
Carl Lewis and Allyson Felix also have ten medals, but have eight golds, one silver and a bronze respectively.
“It is just great,” the 100m and 200m world record holder said. “I’ll continue dominating. I’ll continue to work hard. For me, my aim is to continue into the greatness thing.”
The United States team gave the Jamaicans a scare but Rakieem Salam’s handover to Justin Gatlin left the individual 100m runner-up off balance.
Gatlin clearly strayed into the Bolt’s lane outside him but somehow escaped disqualification.
It made no difference to Bolt, who streaked clear to complete victory in the sixth-fastest time ever.
“I wasn’t really worried about Justin. I knew if he got the baton in front of me, I could catch him.
“So it was just going out there to run as fast as possible,” Bolt added.
Bolt delighted the crowd with a celebratory Cossack dance before parading with his teammates, Nesta Carter, Kemar Bailey-Cole and Nickel Ashmeade, round the track.
His compatriot Shelly-Ann Fraser-Pryce clinched her third gold medal of the competition as Jamaica also won the women’s 4×100m relay. The United States and Britain won silver and bronze respectively as France were disqualified after an appeal against their final changeover.
Carrie Russel, Kerron Stewart, Schillonie Calvert and Fraser-Pryce won in a championship record 41.29secs.
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