In one of the most competitive finals of all time, there was a blanket finish, with the stadium scoreboard initially flashing a photo finish for the first seven athletes.
It then confirmed Lyles as the winner in a personal best 9.79 seconds, the same time as Jamaica's Kishane Thompson, but ahead by a fraction.
If the race had been 99 metres Thompson would have been celebrating, but fast-finishing Lyles kept his form superbly and timed his dip expertly to add Olympic gold to his world title.
He ripped his bib name from his shirt and held it aloft, announcing himself, as he had always promised, as the fastest man in the world.
"It's the one I wanted, it's the hard battle, it's the amazing opponents," said Lyles, the first American Olympic 100m champion since Justin Gatlin in 2004.
"Everybody came prepared for the fight and I wanted to prove that I'm the man among all of them, I'm the wolf among wolves."
Compatriot Fred Kerley took bronze in 9.81 and Akani Simbini of South Africa was fourth, making it a remarkable six fourth or fifth finishes in global championships, albeit with the consolation of a national record of 9.83.
Defending champion Lamont Marcell Jacobs of Italy, heavily strapped, finished fifth in 9.85 and, such was the quality of the race, that eighth-placed Oblique Seville of Jamaica still clocked 9.91 seconds.
It was the first time eight men have broken 10 seconds in a wind-legal 100 metres race.
