Eagle served as the Minister of State for Pensions and Ageing Society from June 2009 until May 2010. Eagle was elected to the Shadow Cabinet in October 2010 and was appointed by Edward Miliband to be Shadow Chief Secretary to the Treasury.
In October 2011, she was appointed Shadow Leader of the House of Commons when Miliband reshuffled his Shadow Cabinet. She was appointed as both Shadow First Secretary of State and Shadow Secretary of State for Business, Innovation and Skills in September 2015 in Jeremy Corbyn's first Shadow Cabinet.
Backbencher and first period as government minister
Eagle was first elected to parliament as member for Wallasey in the 1992 election, defeating by 3,809 votes the Conservative Minister for Overseas Development at the Foreign Office Lynda Chalker.
In parliament she became a member of the Employment Select Committee in 1994, and was promoted by Tony Blair in 1996 to the position of an Opposition Whip, and became a member of the Blair government following the 1997 general election as the Parliamentary Under Secretary of State at the Department for the Environment, Transport and the Regions, moving to the Department of Social Security in 1998.
Eagle voted in favour of the U.S.-led invasion of Iraq in 2003, and repeatedly against investigating it in 2003, 2006, and 2007.
Brown government minister
She returned to the government under Gordon Brown on 29 June 2007 as Exchequer Secretary to the Treasury, the most junior minister at HM Treasury. She was promoted to Minister of State at the Department for Work and Pensions in the June 2009 reshuffle.
In April 2008 Eagle took part in a debate in Parliament on the UK economy in which the Liberal Democrats tabled a motion suggesting that the country was facing an "extreme bubble in the housing market" and the "risk of recession". Eagle responded, "Fortunately for all of us … that colourful and lurid fiction has no real bearing on the macro-economic reality."