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Ms Stokes had been the operations head since July 2013. She was the chief executive at QLDC-controlled Lakes Leisure before that and previously held senior roles at the Auckland Council and Auckland City Council.
Mrs Stokes brought with her experience in senior policy development, planning and project management and had worked in both the public and private sectors, a council statement released on Thursday said.
DCC chief executive Dr Sue Bidrose said she was ''very pleased'' to welcome Mrs Stokes to the team.
''Ruth is a successful general manager with a financial background, strong public service values and a reputation for delivering. Her mix of skills will be an asset to the council.''
Mrs Stokes will begin in Dunedin in February, taking on the responsibilities of Mr Avery, who announced his resignation after acknowledging the buck stopped with him in terms of management responsibility, following the discovery of the Citifleet fraud.