Opposition, 2008–2017

Twyford's first nine years as a Member of Parliament were spent in Opposition. He held a range of urban development and foreign affairs portfolios under successive Labour leaders including development assistance, disarmament and arms control (2008–2011), transport or associate transport (2011–2013, 2014–2017), housing (2013–2017) and building and construction (2009–2011, 2015–2017). In his second term, he was ranked 11th in the shadow Cabinet by leader David Shearer and he continued as a senior member of the Opposition under David Cunliffe and, in Twyford's third term, Andrew Little and Jacinda Ardern.

As an Auckland-based member of Parliament Twyford was appointed to the Auckland Governance Committee which examined the National Government's proposals to consolidate Auckland's eight existing local authorities into one "supercity" governed by the Auckland Council. The Labour Party opposed the reforms. In 2009, Twyford promoted the Local Government (Protection of Auckland Assets) Amendment Bill to address concerns that the council amalgamation was partially to allow the sell-off of public assets. The Bill was defeated at first reading.^[7][8]

A second member's Bill in Twyford's name, the Depleted Uranium (Prohibition) Bill, was selected for debate in September 2010. It proposed a ban on depleted uranium weapons and armour from New Zealand.^[9][10][11] It was debated in June 2012, and failed to advance on a tied vote.^[12]

As housing spokesperson in July 2015, Twyford was criticised for alleged racism when he produced statistics claiming that Chinese foreign buyers were disproportionately buying up real estate in Auckland.^[13][14]

Sixth Labour Government, 2017–2023

Twyford was elected as a Cabinet Minister by the Labour Party caucus following Labour's formation of a coalition government with New Zealand First and the Greens,^[15] and appointed as the Minister of Housing and Urban Development and the Minister of Transport.^[16] In November 2017, Twyford defended his government's proposed Overseas Investment Amendment Act to ban foreign buyers from buying residential property in order to ease the country's housing shortage.^[17][18]

On 24 May 2018, Twyford was dismissed from responsibility for civil aviation (part of the Transport portfolio) after making an unauthorised phone call on a domestic flight as the plane was taking off, a violation of national civil aviation laws. The matter had been raised by Opposition Transport spokesperson Judith Collins. Twyford also offered to resign as Transport Minister but his resignation was turned down by Prime Minister Jacinda Ardern.^[19][20]

On 23 January 2019, Twyford admitted that the Government would not meet its first target of building 1,000 KiwiBuild homes by 1 July 2019, stating that only 300 homes would be built by then.^[21][22]

On 27 June 2019, in Prime Minister Jacinda Ardern's first major reshuffle of the coalition government, Twyford was replaced as Housing Minister by Megan Woods and succeeded David Parker as Minister of Economic Development. He retained the Urban Development and Transport portfolios.^[23]

During the 2020 New Zealand general election, Twyford was the subject of a Facebook attack ad by his National Party opponent Alfred Ngaro alleging that Twyford supported recreational cannabis and unlimited abortion. Though Ngaro subsequently deleted his post, Twyford captured a screenshot and accused his opponent of spreading fake news.^[24] In response, National Party leader Judith Collins issued a media statement that Ngaro's comments did not represent the views of the party.^[25] Twyford retained his seat in Te Atatū by a final margin of 10,508 votes, defeating Ngaro.^[26]

Following the 2020 election, Twyford was dropped from Cabinet but remained a Minister outside of Cabinet as Minister for Disarmament and Arms Control, Minister of State for Trade and Export Growth, Associate Minister of Immigration and Associate Minister for the Environment.^[27]

In a cabinet reshuffle by new Prime Minister Chris Hipkins on 31 January 2023, Twyford lost all his remaining ministerial portfolios.^[28] On 10 February 2023, Twyford was granted retention of the title "The Honourable" for life, in recognition of his term as a member of the Executive Council.^[29]

During the 2023 New Zealand general election, Twyford retained the Te Atatū by a narrow margin of 131 votes over the National Party candidate Angee Nicholas.^[30]

In early November 2023, Twyford condemned violence by both Hamas and the Israeli Defense Force during the 2023 Israel-Hamas war at a Palestine solidarity rally in Auckland. He was booed off the stage by the crowd. Green Party MP Chlöe Swarbrick also spoke at the same rally and expressed support for the Palestinians, chanting "From the river to the sea, Palestine will be free."^[31] In response to controversy around Swarbrick's chant, Twyford stated that he "chose not to [use it] because I think it's unhelpful."^[32]

Sixth National Government, 2023–present

Following the formation of the National-led coalition government in late November 2023, Twyford assumed the shadow immigration, disarmament and arms control, and associate foreign affairs portfolios in the Shadow Cabinet of Chris Hipkins.^[33]