The 150-pupil Lews Castle will join the 940-pupil Nicolson under new management by next August on the Nicolson site.
Councillors insisted the decision was taken for educational reasons. But unions have predicted a clear-out at the Nicolson since the school was embroiled in the bullying row that followed the suicide of a 16-year-old girl.
An HMI investigation ordered by the Scottish Office criticised weaknesses and highlighted "a climate of distrust and suspicion" between the school and the authority. The school board resigned en masse last summer over a further dispute with senior school staff. Senior managers in both schools will now be forced to apply for top posts in the venture.
The council sounded out its plans at eight public meetings and has given guarantees that a strong vocational base will remain.