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Following the Conservative Party's defeat in the 1997 General Election, Howard unsuccessfully made a bid for the post of Conservative Party leader and held the posts of Shadow Foreign Secretary ( 1997 – 1999 ) and Shadow Chancellor of the Exchequer ( 2001 – 2003 ).

In November 2003, following the Conservative Party's Vote of No Confidence in its leader Iain Duncan Smith, he was elected unopposed to the position of Conservative Party leader.

In the 2005 General Election, the Conservatives gained 33 new seats in Westminster, including five from the Liberal Democrats, but this still only gave them 198 seats to Labour's 355.

Following the election, Howard resigned as Leader of the Conservative Party and was succeeded by David Cameron.

Howard did not contest his seat of Folkestone and Hythe in the 2010 General Election and entered the House of Lords as Baron Howard of Lympne.