Fleming's resignation bring to an end one of the most successful tenures as a coach with the Super Kings winning five IPL and two Champions League T20 (CLT20) titles.
The 53-year-old also ended ties with Super Kings' other franchises - Joburg Super Kings (SA20) and Texas Super Kings (MLC) - where he was head coach.
"Eighteen years is a lifetime in sport, and I leave with nothing but gratitude," Fleming said in a statement. "My time with Chennai Super Kings has been the privilege of my coaching career.
"I am proud of everything we have achieved. Together, we celebrated unforgettable victories, overcame difficult moments, and built memories that will stay with me forever.
"CSK will always be close to my heart, and I will be cheering the team on for years to come."
Fleming joined CSK as a player ahead of IPL 2008 and took over as head coach the following season. He formed a formidable working relationship with MS Dhoni and helped the team enter the playoffs a record 12 times.
They also made a record ten appearances in the final, and won titles in 2010, 2011, 2018, 2021 and 2023. They won the Champions League title in 2010 and 2014.
Joe Root has made it known that he accepted the England Test captaincy because he wanted to work with new coach Stephen Fleming to "build something pretty special together".
England managing director Rob Key admits he "wouldn't be surprised" if Ben Stokes reverses his retirement and returns to the Test team ahead of next year's home Ashes.
The England and Wales Cricket Board has appointed Stephen Fleming as the England Test Head Coach, while veteran Joe Root has been named captain.
Royal Challengers Bengaluru CEO Rajesh Menon is sure India legend Virat Kohli will remain with the franchise and play IPL cricket for "at least four years".
