Mr Millham has long been a bete noire of union activists and his departure coincides with an initiative by the college's board of management to improve relations with staff after a series of setbacks.
A board statement, issued through Beattie Media, its public relations consultant, said: "Richard has had a long and distinguished career in further education and in the last 12 years has led the college in a period that has resulted in its significant development and success."
Motherwell College now has 19,000 learners and has achieved Investors in People status.
In June, the board launched a review of staff relations after Douglas Nicol, then branch convener of the College Lecturers' Association, was awarded pound;44,500 at an employment tribunal after managers were deemed to have unfairly demoted him. Mr Nicol had been accused of "wilfully disregarding his duties".
The union, now fully part of the Educational Institute of Scotland, has pointed out that it was the sixth decision to go against the college in five years.
The move to cement relations comes after repeated union allegations of bullying and harassment.