The northbound carriageway was closed at 02:00 on Thursday at junctions five, Castle Bromwich and six, Spaghetti Junction and was not reopened until about 01:30 GMT on Friday.
A 26-year-old man driving a Saab died at the scene.
A 200m-length section across four lanes had to be resurfaced after a fuel spillage, Highways England said.
Read more on this story and other news from Birmingham and the Black Country
A Highways England spokesman said earlier: "You've got about a 200m stretch - so that's 800m across all four lanes.
"Fuel has leaked on to the carriageway and it's really got into the carriageway, so that's the problem and it's just not safe to reopen."
Traffic jams trailed back to junction four for the M42.
Drivers were stuck for hours in congestion on the M42 north from junctions six to nine and on the A446 around Coleshill.
Many of the main routes into Birmingham slowed to a crawl as people tried to find alternative routes.
BBC Travel has the latest
Two southbound lanes between junctions six and five, that were closed at about 03:00, reopened about six hours later.
Two lanes closed on the northbound carriageway of the M6 at junction 3A near Coleshill after a separate traffic collision at 12:30 reopened by 13:00, said Highways England.
Drivers expressed their anger on social media at being caught in the congestion in and around Birmingham during Thursday's rush hour.
Paul Davis tweeted at 10:00 he had only managed to drive six miles after leaving from Sutton Coldfield at 07:00.
Earlier Virgin Trains said it had advised its ticket managers at Birmingham International to use discretion towards commuters in light of the disruption.
Police had hoped to reopen the northbound lanes at about 07:30 on Thursday, but Highways England said extensive damage had been caused and assessment and repair work was being carried out.
Diversions were put in place but motorists were caught up in long delays on surrounding routes, particularly on the A38.
West Midlands Ambulance Service said the lorry driver in the collision was shaken but uninjured.

Kluber struck out eight of the first nine outs registered and Roberto Perez hit two home runs as the Cubs endured a miserable return to the season finale.
The Cubs' last World Series win was in 1908, while the Indians clinched their most recent title in 1948.
Game Two of the best-of-seven series begins at 00:08 BST on Wednesday.
The first pitch has been brought forward an hour because of the threat of rain in the Cleveland area.

The Standing Rock Sioux Tribe hailed an "historic decision" and said it was "forever grateful" to President Obama.
Instead, the US Army Corps of Engineers will look at alternative routes, a statement by the campaigners said.
The Sioux have been protesting since April against the pipeline which is near a reservation.
"Today, the US Army Corps of Engineers announced that it will not be granting the easement to cross Lake Oahe for the proposed Dakota Access Pipeline," the tribe's statement read.
"Instead, the Corps will be undertaking an environmental impact statement to look at possible alternative routes."
The multi-billion dollar pipeline, which runs close to the Standing Rock Sioux Native American Indian reservation, is nearly 1,200 miles (1,900km) long.
It is nearly complete except for the lake section.
The Dakota Pipeline stand-off explained
The Sioux, along with other Native Americans, oppose the pipeline because they fear it will contaminate drinking water and run over sacred burial sites.
Hundreds of US military veterans joined the activists last week. The campaigners, who have numbered thousands, have endured bitter temperatures and had been ordered to leave the area by Monday.
President-elect Donald Trump, who has had stocks in Texas-based Energy Transfer Partners, the project's builder, and Phillips 66, which owns one-quarter of the pipeline, has said he supports the project.
But he denies his policy is related to any financial interest.
North Dakota Republican Representative Kevin Cramer said the Army Corps' decision amounted to "a very chilling signal" for US infrastructure.
North Dakota Governor Jack Dalrymple called the decision a "serious mistake".
The protests, on federal land, have seen clashes between the demonstrators and law enforcement.
Part of the M6 in Birmingham was closed for almost 24 hours after a fatal collision involving a lorry and a car.
[NEXT_CONCEPT]
A superb pitching display from Corey Kluber helped the Cleveland Indians to an emphatic 6-0 win over the Chicago Cubs in the World Series opening game.
[NEXT_CONCEPT]
The US Army has decided not to allow an oil pipeline to cross under a reservoir on land it controls in North Dakota in a move praised by protesters.