Chief executive Rod Taylor and vice-chairman Graham Hodgson have both relinquished their roles just three weeks after fellow director Stephen Wright also stepped down.
Taylor is set to continue on the board in a lesser capacity but Hodgson will not have any involvement, ending a 22-year association with the Shrimps.
Taylor told the Morecambe Visitor: "The complexion of the football club has changed over the past four years with executive directors being employed and I have felt that the title of CEO has been a misnomer for quite some time now.
"The title is appropriate for someone who is shaping the way the company operates on a day to day basis and under the changed regime I have not been able to perform that function for a number of years."
Hodgson said: "Unfortunately, at the present time, I am not entirely comfortable with how the company is being managed and for this reason I have tendered my resignation."