Winter re-joined the Terriers as CEO in Easter 2016, having previously worked in that role at Sheffield United.
He also worked in a similar capacity at Watford.
The 54-year-old has given notice of his intention to vacate his role at Town, with his leaving date currently projected to be in March 2020.
Town chairman Phil Hodgkinson commented: "I would like to thank Julian for his work on behalf of the club.
"I have only worked with him for a relatively short time, but I am particularly grateful for the groundwork he put into the period of my takeover.
"He now feels it is time for a new challenge and we fully respect his wishes. I know he will continue to work diligently in the best interests of our club while we complete the process of appointing his successor.
“The search for the club’s next chief executive is now well under way and is obviously a very important one.
"We will take our time, as we did with our recent appointment of Danny and Nicky Cowley, to ensure the correct appointment is made.”
Huddersfield-born Winter represented his hometown club in his playing career, progressing through the youth system to play over 100 games for Town between 1984 and 1989.