The Dutchman started the race needing to outscore Charles Leclerc and Sergio Perez by eight and six points respectively, but a first-lap crash and intensifying rain meant the race was suspended for more than two hours and put at risk of not restarting.
But with around 45 minutes to go the weather cleared enough to get the race back underway with a rolling restart.
Verstappen controlled the restart beautifully, and after a pit stop a handful of laps later to switch from full wets to intermediate tyres he started to pump in fastest laps.
He broke from the field at more than a second a lap to put victory beyond doubt long before the end of the 28-lap time-limited race, which he won by a crushing 27 seconds, but his championship victory was far from assured with Leclerc in second and Perez in third.
In those positions Perez would be defeated by Leclerc would go to the next race in Austin still in contention by a point.
But as the race wore on, Leclerc struggled increasingly to keep his tyres alive around the demanding circuit, and Perez began to bear down on him.
With five laps to go they engaged, but Leclerc’s defensive work despite his ailing rubber was commendable in clinging to the place.
But his hard work was undone at the final chicane, where he outbraked himself and ran deep. He rejoined the track and crossed the line just ahead of Perez but had cut the track to hold the position, and the stewards immediately put him under investigation.
It took just minutes for them to rule in Perez’s favour, swapping their positions on the podium and thereby handing Verstappen his second championship - despite some confusion over whether reduced points would be awarded for less than 75% of the race being completed, though these regulations apply only in the case of a suspended race.
“Incredible of course!” Verstappen said, having been told partway through the post-race interviews that Leclerc’s penalty had handed him the title. “It’s very special also to do it here, in front of all the Honda people, all the Japanese fans.
“It’s crazy, mixed emotions. Winning the race, but looking back - what a year we’ve had. It’s been incredible.
“I’m so thankful to everyone who has worked so hard. The work we’ve done together with Honda, to win twice with them is so emotional, especially here. I’m very proud we could do it here.
“Just the season we’ve had, the one-twos, leading the constructors [championship] - it’s been a special year, and you need to remind yourself as these kind of years you don’t have very often.”
Esteban Ocon finished an excellent fourth after a race-long battle to hold position from Lewis Hamilton, who was among the most eager to get the race going after the long rain suspension, though the Mercedes driver couldn’t break through the Alpine’s defence.
Sebastian Vettel scored a sensational sixth despite dropping to last with a spin on the first lap. A tyre gamble at the restart, being the first to switch from full wets to intermediates, rocketed him up the order, and an excellent defensive drive had him hold the place ahead of Fernando Alonso and score points in his final Japanese Grand Prix before retirement.
George Russell recovered from 11th to eighth after a slow pit stop with a trio of sublime overtakes around the outside of the esses.
Nicholas Latifi scored his first points of the season with ninth ahead of McLaren’s Lando Norris in 10th.
The race was surprisingly tame after the resumption despite the chaos of the original start which saw Carlos Sainz crash out of the race in treacherous conditions and Thai driver Alex Albon stop with a technical problem.
The safety car was subsequently deployed to recover the cars, but the recovery truck was sent onto the track before the field had bunched up behind the leader.
Pierre Gasly was still making up ground after a first-lap pit stop for repairs and was speeding past the scene of the crash when the truck appeared through the thick mist.
The Frenchman was travelling at around 200 kilometres per hour at the time and was furious with race control’s handling of the situation.
Other drivers were also appalled even as they trailed behind the safety car while crossing the crash scene, noting the low visibility and slippery conditions made it extremely dangerous in the event any river lost control or were caught unsighted.
“I was going flat out!” Gasly was overheard saying during the subsequent stoppage. “I could have f***ing killed myself.”
The FIA defended its use of the recovery vehicle while cars were on track, noting its standard procedure if the safety car is in control of the race.