Nathan Thompson, who spearheaded the strategy to develop 450 acres on Edinburgh's waterfront, has "left to pursue other business interests", a spokesman for the firm said.
The sale of the shopping centre is an option that Arcus European Infrastructure Fund is understood to be considering as it prepares to take full ownership of the business next month following necessary court approvals.
A property insider said that Arcus was in discussions with agents over plans to "sell the shopping centre and some adjacent land".
The board of the ports group, led by Charles Hammond, accepted a 745 million offer from Arcus, its biggest shareholder, in March.
But while Hammond and his new finance director, Stuart Paterson, will stay with the business, Thompson was put on gardening leave last week. Documents at Companies House yesterday revealed he has resigned as managing director of Forth Property Developments.
The news of the "well-respected" Thompson's departure came as a shock to the Edinburgh industry.
It is thought his departure was due to Arcus's plan to develop "new partnerships" to shape the direction of the firm's property business.
One property insider said: "I'm surprised that Nathan has left. One, he knows the portfolio inside out.
"And two, if they are planning on disposing chunks of it I would have thought it would be useful to have him there for that part of the process."
Roy Durie, a consultant with property firm Ryden, said: "Nathan Thompson is very professional. They will miss him. I'm sad to see him go."
Thompson joined Forth Ports in 2004 as deputy property director, succeeding to the top job following the retirement of property director Terry Smith in 2006.
He led the development of the Leith Docks masterplan, the largest in the history of Scotland, which won approval from City of Edinburgh Council in 2008.
But the recession plunged the Forth Ports property division into torrid times. In 2008, the value of the firm's property portfolio collapsed and undermined his 30-year plan to build 15,000 town-houses and flats in the site in a series of nine "urban villages".
The first of these is the Harbour development, which Forth Ports said was set to win detailed planning consent from the local authority.
In its final year-end results as a publicly listed company in March, Forth Ports said its property division had made "good progress" in finding new tenants for Ocean Terminal despite the downturn and the disruption due to tramworks.In 2009, the firm bought out its joint venture partner in the shopping mall, HBOS, for 2m, and said Ocean Terminal had an estimated market value in 2009 of 85m.
A spokesman for Forth Ports said it was "company policy not to comment on rumours and speculation of this nature".