Favourite in 2022, Norway's Ingebrigtsen was outkicked by Britain's Jake Wightman to miss out on gold and Kerr, the Tokyo Olympic bronze medallist behind Ingebrigtsen, made his move at about the same spot with 200 metres to go.
Kerr dug deep to stay in front and won in 3:29.38 with Ingebrigtsen, whose 3:27.14 run in Poland five weeks ago made him the fourth-fastest man in history, taking silver in 3:29.65.
Fast-finishing Norwegian Narve Gilje Nordas secured the bronze in 3:29.68.
"It's been a long time coming. It's quite an overwhelming experience. I'm so proud of myself," said Kerr, who ran the race in sunglasses.
"I didn't feel like I ran the best race either. I just threw my whole 16 years of this sport in that last 200m and didn't give up until the end.
"But it would scare you how meticulously we planned for this. We threw everything we had at this in terms of nutrition, sleep, training, race reviews, everything.
"We left no stone unturned and if it wasn't a gold medal today, that was the best we could have done. And so I planned like a champion and I was able to do that for myself today."
Kerr had a good view of Wightman's tactics in Eugene as he chased him home to finish fifth and he produced an almost uncanny replica of his Edinburgh club mate on Wednesday.
"As I came round the bend I thought I have to give everything I have. I just made sure I was there with 200m to go," he said.
"Then in the last 30, I thought 'I want this so badly, I don't care how much pain I'm in I'm going to do everything to get to the finish line first'."
Ingebrigtsen said he was not physically in great shape as he was unable to respond to Kerr moving onto his shoulder.
"All credit to Josh, he had a good race, but I feel a little bit unlucky not being able to do what I have been doing the whole season," he said.
"I was a little bit dry in my throat, it got worse last two days. I don't feel my body was quite 100%.
"I won't blame it on anything, but last year I was by far the best, but did a worse race. But today I wasn't the best.
"I'm disappointed, but not when others do things right and are as prepared as they are. I don't feel like I could have done much differently."
Last year Ingebrigtsen recovered to win the 5,000m gold and he has the chance to do that again in Budapest.
Dominican Republic's Paulino claims 400m gold
Marileidy Paulino (26) of the Dominican Republic won World Championship gold in the women’s 400m on Wednesday, finally claiming top spot on the podium after silvers at last year’s worlds and Tokyo Olympics.
The race was wide open in the absence of injured American Sydney McLaughlin-Levrone, the 400m hurdles world record holder and fastest in the world this year over the flat, and with Olympic and defending world champion Shaunae Miller-Uibo going out in the heats four months after having a baby.
Paulino, second-fastest in the world this year, knew she would never get a better chance to become the first Dominican female world champion and did not waste it.
Dutchwoman Lieke Klaver set the early pace but faded on the final bend and was swallowed up.
Paulino was out in lane seven and ran a controlled race to surge ahead at the top of the home straight and drive home for an emphatic victory in a national record 48.76 seconds.
Poland's Natalia Kaczmarek finished strongly to take silver in 49.57 followed by Sada Williams of Barbados, who matched her bronze from last year, with 49.60.
"A lot of emotions are rushing through me," Paulino said.
"This national record means a lot to me. It is really incredible, but I have been preparing for this for a long time, working hard to achieve a goal like this.
"The gold medal was my dream, and I had the talent to turn this dream into reality."
Kaczmarek said the key to her second-place finish was to concentrate on her own performance.
"This race was crazy, they were so fast out of the blocks," she said.
"My coach had said to me: 'Be careful, keep your pace, run your race'. I did it but it was very painful. This pain after the race is huge, but the joy is better.
"That is first world championships medal for Poland over 400m. It is still difficult to believe that this silver medal is mine."
