It is understood concerns have been voiced in museum circles about Mr Ingram's departure, and a petition signed by some museum staff was circulated to support him.
Museum director Linda Wigley acknowledged "the tremendous work that John has done at the museum" and wished him well for the future.
She declined to comment on the circumstances involving his departure and said she had not seen any petition.
Mr Ingram (55), who also declined to comment on his reason for leaving, stepped down last week.
A former primary school principal, he has been on the museum staff for the past seven years, initially job-sharing.
He has been closely involved with the growth of the museum's successful "Walk Dunedin" programme, which now offers guided walks of the city seven days a week.
Mr Ingram has also co-ordinated a range of popular visitor programmes, including railway jigger races, public parades involving historic fire engines, and the museum's Pixie Town activities.
He said he had enjoyed his work at the museum and was "very proud" of the calibre of the volunteer guides.
"Their contribution has made Walk Dunedin the success that it currently is," he said.
He was also grateful for the strong support gained from fellow staff and the community throughout his employment.
The settlers museum and Dunedin Public Art Gallery are owned and operated by the Dunedin City Council.
