Sir Keir Starmer reshuffled his top team on Monday, giving his deputy a long-awaited more high profile role in his shadow cabinet.
It follows calls from some Labour MPs to give Ms Rayner “a proper job to get her teeth into” rather than her previous roles as shadow secretary of state for the future of work and chancellor of the Duchy of Lancaster.
She will now oversee a major departmental brief opposite Michael Gove. Ms Rayner was directly elected to be deputy leader by party members, meaning she keeps that position no matter what.
The Labour leader’s shake-up came as MPs returned to Parliament after the summer recess and saw the promotion of a number of Blairite MPs.
Hilary Benn was appointed shadow Northern Ireland secretary, while Pat McFadden was promoted to the chancellor of the Duchy of Lancaster and national campaign coordinator roles.
Peter Kyle, who worked as a special adviser in the Cabinet Office under Blair, was moved to oversee the science, innovation and technology brief.
Liz Kendall was promoted to shadow work and pensions minister, having previously held the social care minister brief.
Meanwhile Croydon North MP Steve Reed was pushed out of his shadow justice secretary role and replaced by Shabana Mahmmod, who had impressed MPs in her previous role as national campaign coordinator.
Rosena Allin-Khan was out as shadow mental health minister.
“You made clear that you do not see a space for a mental health portfolio in a Labour cabinet,” she said in a letter to Sir Keir.
Jim McMahon was the first to go on Monday morning, stepping down from his shadow environment secretary post, which was handed to Mr Reed.
The Oldham MP said he remained “a firm supporter of Keir and the project we have built to offer Britain an electable Labour government”.
Thangam Debbonaire was handed the shadow culture, media and sport secretary role, replacing Lucy Powell who was appointed shadow leader of the House of Commons.
The Labour leader’s was not expected to move his most senior team, with shadow chancellor Rachel Reeves, shadow health secretary Wes Streeting and shadow home secretary Yvette Cooper all staying put.
It comes as the school crumbling concrete scandal prompted Labour to revive its series of controversial attack adverts on the prime minister .
A new poster on Sunday featured Rishi Sunak face alongside the tagline: “Do you think your child’s school should be safe? Rishi Sunak doesn’t.”
It follows similar ads earlier this year, which had accused Mr Sunak of not wanting child sex abusers to be jailed.
The Government is also facing another awkward by-elections later this year.
Tory former whip Chris Pincher has lost his appeal against an eight-week suspension from the Commons following allegations he drunkenly groped two men at London’s exclusive Carlton Club last year.
It paves the way for a potential by-election in his Tamworth seat.
Ministers on Monday are also expected to move the writ to hold a vote in Mid Bedfordshire, the seat vacated by Nadine Dorries.
The Liberal Democrats are favourite to win the formally safe Conservative seat.
The party’s chief whip Wendy Chamberlain said: “The Conservatives have left the people of Mid Bedfordshire without proper representation for over a year. Rishi Sunak wanted to delay another humiliating defeat for the Conservative Party for as long as possible and we forced his hand.”
Mr Sunak had a mini Cabinet re-shuffle last week in which he avoided major changes but gave new appointments to close allies Grant Shapps and Claire Coutinho.
Some expect the PM to carry out a wider Government reshuffle in the coming months.
Both leaders are now gearing up for annual party conference season in October and look to getting their top teams in shape for the next general election, expected next year.