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Cam McCracken took on all three roles in an acting capacity in August last year, following the resignation of former museum director Jennifer Evans.
Today that was made official.
Dunedin City Council ara toi group manager Nick Dixon said Mr McCracken had done "a great job'' in the acting position.
Mr Dixon said at one stage it was thought Toitu would retain its own director post, but over the past year it became apparent the roles could be combined.
Having integrated leadership across city museums and galleries was nothing new, and happened internationally.
Staff had worked with the Otago Settlers Association and the Dunedin Chinese Gardens Trust, and those organisations had been advised of the decision to have a combined leadership post.
Mr McCracken, who has been art gallery director since 2012, said he was delighted to take on what he described as a challenging role.
Closer integration would allow the institutions to make an even stronger contribution to Dunedin's development.