The 1997 Formula 1 champion and 1995 Indianapolis 500 winner has not competed at NASCAR's top level since a handful of outings in 2007 and '08 with Bill Davis Racing.
He will attempt to qualify Braun Racing's #32 Toyota at Indy after a successful race with the team in the Nationwide Series at Elkhart Lake recently.
"I am very excited to join with Braun Racing and [sponsor] Dollar General at Indianapolis," Villeneuve said.
"We had a very exciting and solid race last month at Elkhart Lake. I had hoped it would result in additional opportunities to drive for the organisation.
"I have a lot of good memories at the Brickyard. Winning the Indy 500 was a very big highlight in my career. This will be my first venture in a stock car there, but I am confident that we will do well."
Team owner Todd Braun was delighted to have Villeneuve in his car for Indianapolis.
"Entering the Brickyard 400 as an owner at this historical track means a lot to me," he said. "It is extra special because I grew up here in Indiana.
"It's also exciting to take a former Indy 500 winner to the Brickyard. He and Trent [Owens, crew chief] work very well together, and I know that Trent is looking forward to the feedback that Jacques can provide him.
"He is an extremely talented driver. Jacques is a great asset to our team."
If Villeneuve qualifies for the race, he will join Juan Pablo Montoya as the only driver to contest all three of Indianapolis' major car racing events - the Indy 500, United States Grand Prix and Brickyard 400.
Marcelo - Jose a born winnerVilleneuve to return to Nationwide
