He was promoted to the frontbench by Neil Kinnock in 1988 as a spokesman on trade and industry, until he moved under the new leadership of John Smith to serve as a spokesman on the environment in 1992. Following Smith's death in 1994 he was moved by Tony Blair to become the Deputy shadow Leader of the House of Commons and spokesman on John Major's citizens' charter. In 1995, he became a home affairs spokesman. When the first Blair government was elected at the 1997 General Election he was made a Minister of State at the Foreign and Commonwealth Office with the brief of Minister for Europe, before moving to the Ministry of Defence in 1998 as the Minister for the armed forces. He was sacked in 1999 amid speculation that his close association with and perceived loyalty to the Chancellor of the Exchequer Gordon Brown eventually cost him his government job, and he became an increasingly outspoken backbencher. In May 2006, Henderson joined other Labour MPs in urging Prime Minister Tony Blair to set a date to step down following the dismissal of Charles Clarke as Home Secretary. He stated that "Quite frankly, Tony Blair has done his bit and it is now time for him to tell us when he is going to go." He is the vice chairman of the all party groups on the Philippines; Malaysia; and the chocolate and confectionery industry. He spoke in favour of government plans to replace Trident in the debate on 14 March 2007.