The Olympic bronze medallist pulled off a perfect tactical race, forcing the Norwegian into a change of pace on the last lap and taking victory in a time of 3:29.38.
Crossing the line with his rivals a stride behind, the Edinburgh star cupped his hand to the crowd and roared in celebration as the great Seb Coe draped a gold medal over his neck.
Kerr followed in the footsteps of 2022 gold medallist Jake Wightman in bringing down Ingebrigtsen and became the third British man to be crowned world champion over the metric mile.
"I just threw my whole 16 years of this sport in that last 200 metres and didn't give up until the end," said Kerr. "I'm so proud of my team and my family – they got me here.
"I didn't feel like I ran the best race either! I was battling with Jakob pretty hard and throwing everything I could at the guy.
"We were both hurting and I was just like, 'I've wanted this for my whole life and I'm not letting anyone get in the way of that.'
"I'd be proud if giving everything I had in this situation if that was gold, silver, bronze. But I've had the bronze and the gold is a lot sweeter
Ingebrigtsen looked to dominate the race from the front within the first lap alongside Kenya’s Abel Kipsang, with Britain's Neil Gourley on the inside and Kerr a couple of strides behind him.
Kerr took closer order as they went round for the penultimate lap, slowly gaining and right alongside the Olympic champion as they took the bell.
Just as Wightman had done a year earlier in Eugene, Kerr struck for home with around 200 metres to go and broke Ingebrigtsen as they came down the straight.
Having finished sixth and fifth in his last two World Championship finals, Kerr took victory by 0.27 seconds with Ingebrigtsen settling for silver in 3:29.65 and fellow Norwegian Narve Gilje Nordas claiming bronze.
National Lottery players raise more than £30m a week for good causes including vital funding into sport – from grassroots to elite. Find out how your numbers make amazing happen at: www.lotterygoodcauses.org.uk #MakeAmazingHappen #ThanksToYou