The Canadian made his series debut in 2022 with Andretti Autosport and continued with the team into 2023 before losing his seat.
Now, DeFrancesco will return with Rahal Letterman Lanigan Racing.
DeFrancesco, who won the LMP2 class in the 2022 Daytona 24, will pilot the #30 entry alongside Graham Rahal and series rookie Louis Foster.
“I’m very excited to be back in the IndyCar Series,” said DeFrancesco.
“Rahal Letterman Lanigan Racing has an amazing history and is also on an impressive trajectory.
“Seeing all the work that is going on from the men and women behind the scenes, it is easy to see that this team and myself are very hungry for results.
“I look forward to getting started with all the great people here.”
Across his 34 races, DeFrancesco has a career-best IndyCar finish of 12th.
Team co-owner Bobby Rahal welcomed the 24-year-old back to the series.
“I’m very pleased that we are able to welcome Devlin to the team,” said Rahal.
“We had the chance to witness his ability while he was at Andretti and there were clearly times when he was quite competitive so I’m confident that we can have a lot of good races together.
“We’re looking forward to his contribution to the team.”
The announcement leaves just three seats unaccounted for on the 2025 grid.
One vacancy exists at Juncos Hollinger Racing while both Dale Coyne Racing seats remain unaccounted for.
The 2025 season gets underway on the streets of St Petersburg on March 3.
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