The Brit lost his full-time seat with Juncos Hollinger Racing at the end of last season, despite impressing during his time with the team.
But he was given the chance to race with Arrow McLaren in the opening round of the new campaign after David Malukas sustained a wrist injury in a pre-season mountain biking incident, Ilott going on to take 13th in the Grand Prix of St. Petersburg.
Ilott also deputised in the non-championship round at The Thermal Club before his commitments in the World Endurance Championship opened the door for Theo Pourchaire to substitute for Malukas at Long Beach.
However, with Malukas and Arrow McLaren splitting and his replacement Pourchaire skipping the Indy 500, Ilott's services have been called upon once more.
“It is any driver’s dream to race in the Indianapolis 500, and I’d like to extend a thank you to Zak, Gavin [Ward, team principal] and Tony [Kanaan, sporting director] for making this happen," said Ilott, fresh from an historic victory at the WEC Spa 6 Hours in the #12 Jota Porsche.
"I’m grateful to step into this race with a familiar car and a familiar team now in Arrow McLaren. While our April Open Test at the Indianapolis Motor Speedway was shortened by weather, the runs we did have were productive.
"I feel comfortable with the team and know that we can come together throughout the Month of May to put our best foot forward come race day.”
Ilott was the second-biggest mover in last year's running of the race with JHR, climbing 15 positions from 27th to finish 12th.
He will join a four-car effort for Arrow McLaren at the Indianapolis Motor Speedway, joining series regulars Pato O'Ward and Alexander Rossi as well as Kyle Larson, who will be making a tilt at a double with the NASCAR Coca-Cola 600 on the same weekend.
Ward added: “Callum brings experience with this team and at the Indy 500 that we think is very valuable as we enter the biggest two weeks of our season.
"He and the team got along well during the first two events of the season, and we’re looking forward to carrying that over here.
"I’m confident that Callum and the #6 NTT DATA Chevy team will be competing near the front of the grid during qualifying and on race day, just like the rest of our cars.”