After Fianna Fáil's landslide victory at the 1977 general election, Burke was appointed Minister of State at the Department of Industry and Commerce.
Burke was subsequently a staunch and vocal defender of Haughey during several internal heaves against the latter's leadership of the party.
In October 1980, Burke was promoted to Minister for the Environment, a position he held until June 1981 and again in the short-lived Fianna Fáil government of 1982.
After Fianna Fáil returned to power at the 1987 general election, Burke served as Minister for Energy, where he made controversial changes to the legislation governing oil and gas exploration.
Following the 1997 general election, Fianna Fáil was back in office, and Burke was appointed Minister for Foreign Affairs, by Taoiseach Bertie Ahern.
Within months of his appointment as Minister for Foreign Affairs, allegations resurfaced that Burke had received IR£80,000 from a property developer regarding the former Dublin County Council.
An interim report of the Flood Tribunal found as fact that the backers of Century Radio had paid large bribes to Burke to secure favourable ministerial decisions.
Burke has maintained a low profile since completing his prison sentence but attended the state funeral of Charles Haughey in June 2006, his political patron.