The 24-year-old Munster playmaker impressed in cameo appearances at the Rugby World Cup last year, which ended in a heartbreaking 28-24 quarter-final defeat to New Zealand and the culmination of Sexton's stellar 118-cap career.
Crowley must steer titleholders Ireland past their predecessors as champions France - who are without their talisman Antoine Dupont after he opted to prepare for Sevens duty at the Paris Olympics - in the febrile atmosphere of Marseille.
However, head coach Andy Farrell said Crowley has shown he is capable of recording a memorable triumph over a side also bidding to bounce back from the shattering disappointment of a World Cup quarter-final exit.
"He's a confident kid, Jack, so being able to grab hold of the team has been one of the things that has most impressed me during camp," Farrell said at a press conference after naming the team at a training camp in Portugal.
"It's tough for young kids, especially with responsibilities like in his position but he feels very comfortable in being able to do that.
"How you run a week is pretty important and you're making sure that the rest of your teammates feel that you're in control.
"He's obviously learned a lot from Johnny in that regard."
Farrell has opted for a 6-2 forwards to backs split and Crowley will be backed up from the bench by Leinster's Ciaran Frawley, who is primarily a centre but also has experience at fly-half.
Farrell, who will step back temporarily as head coach next year to take the same role for the British and Irish Lions for the tour of Australia, said there would be no radical change to the team's post-Sexton offensive strategy.
"I think what we worked hard with Johnny over the last four years was everyone around him taking responsibility," said the 49-year-old Englishman.
"I certainly feel that we've come on in leaps and bounds in that regard.
"No longer are we just reliant on the 10 to steer the ship, you look at the progression in the last four years."
'Are we brave enough?'
Crowley will have Jamison Gibson-Park alongside him at scrum-half while Munster veteran Conor Murray, who for so long was Sexton's halfback partner and still a reliable pair of hands at 34, is on the bench.
Another Munster man, Peter O'Mahony, captains the side with James Ryan - the player who many thought was being groomed to replace Sexton as skipper - among the replacements.
The lock's dip in form at the World Cup seems to have counted against him with regards to the captaincy, and his Leinster teammate Joe McCarthy will take his place in the second row partnering Tadhg Beirne.
Farrell - who was compensated for the World Cup disappointment by being named world coach of the year - said McCarthy has been impressing him for long while.
"It's not post-World Cup, it was during the World Cup as well and before that actually," he said.
"It's what we see in training and progression etc, and what the other lads see also.
"He's a young fella that's on a mission, he's there to take his chance and his opportunity when he can, and he tends to do that most days."
With outstanding Australia-born wing Mack Hansen ruled out of the tournament, Farrell has opted for Munster's Calvin Nash to start and will win just his second cap.
Another change forced upon Farrell comes in the centres with Garry Ringrose ruled out with a shoulder injury. Robbie Henshaw, no stranger to injuries himself, will partner Bundee Aki.
Farrell says he cannot wait for the whistle on Friday.
"The exciting thing for me is are we brave enough, have we got enough courage to go and do what we said we're going to do?" he said.
"If you want to be successful, if you want to try to be the best, then you've got to beat the best in places like this and the occasion doesn't get much bigger."
Team:
15-Hugo Keenan, 14-Calvin Nash, 13-Robbie Henshaw, 12-Bundee Aki, 11-James Lowe, 10-Jack Crowley, 9-Jamison Gibson-Park, 8-Caelan Doris, 7-Josh van der Flier, 6-Peter O'Mahony (captain), 5-Tadhg Beirne, 4-Joe McCarthy, 3-Tadhg Furlong, 2-Dan Sheehan, 1-Andrew Porter
Replacements: 16-Ronan Kelleher, 17-Cian Healy, 18-Finlay Bealham, 19-James Ryan, 20-Ryan Baird, 21-Jack Conan, 22-Conor Murray, 23-Ciaran Frawley
