Caley Thistle announced Cameron had "retired" after six years in the role, during which they lifted the Scottish Cup for the first time.
"It is time for me to step down and leave others to take the club forward," he said in a club statement.
"I urge the public of Inverness to strengthen their support for the club."
First-team manager Richie Foran said on Saturday he expected to hold talks with the board about his future early this week.
The Irishman was promoted from player to manager on a four-year deal last summer, when John Hughes left after a major disagreement with Cameron.
Cameron's spell as chairman also included a Scottish League Cup final defeat, three top-six finishes and qualification for European qualification for the first time.
But the team were relegated on Saturday after finishing bottom of the Scottish Premiership, one point behind Hamilton Academical, despite a 3-2 last-day win over Motherwell.
"When my appointment as chairman was announced in September 2011, it was described as 'a short-term arrangement'," recalled Cameron.
"This 'short-term' arrangement has lasted almost six years and, due to financial restrictions, I also found myself taking on the role of chief executive as the funds were not available to fill the post.
"It has been my privilege to support the club in a variety of roles as we continued our eventful journey.
"We have experienced periods of exceptional success over the years and for a club, still in its infancy, to achieve what we have on limited resources makes that success all the more remarkable.
"It is never an easy task to remain competitive and successful on limited funding whilst remaining debt free, and it is always a difficult pathway to navigate."
Foran has expressed his desire to stay in post, saying he was looked forward "to getting rid of a few bad apples" from the Highland club's dressing-room.
Kenny Cameron has stepped down as Inverness Caledonian Thistle chairman following his club's relegation from the Scottish Premiership.