In 1987, McGonagle became the only curator to be shortlisted for the Turner Prize thanks to his work at the Orchard Gallery in Derry. The gallery was known for bringing the work of significant international artists to Derry as well as promoting Irish artists, such as Willie Doherty, abroad.
McGonagle became the first director of the Irish Museum of Modern Art when it opened in 1991, but after reported arguments with the chairwoman of the board, Marie Donnelly, he stepped down in 2001. He subsequently took over as director of the City Arts Centre in Dublin.