The Department for Transport is opening a Midlands HQ and northern hub under new investment plans.
The DfT said it would launch a new regional head office in Birmingham and hub in Leeds with an initial 650 roles to be based across the two sites by 2025.
It said these were the latest steps in the Government's drive to move 22,000 civil service roles out of London to communities across the UK by 2030.
The Birmingham base will include new ministerial offices, with ministers expected to spend a significant amount of time there.
Recruitment for both sites is already under way and 100 roles have been created so far, according to the department, including senior civil servant positions which would otherwise be based in London.
The specific locations for the offices have not yet been announced nor what the split of jobs will be across the two cities.
Transport Secretary Grant Shapps said: "This is a historic move for the department and part of a significant wider culture change across Whitehall.
"Transport is absolutely vital to the local communities we serve and having hubs in major cities like Birmingham and Leeds will offer a fresh perspective on how we can better serve these areas."
Transport Minister Chris Heaton-Harris added: "Our department has a key role to play in this Government's drive to level up across the country and having hundreds more roles based outside of London will not only bring an economic boost for Birmingham and Leeds but also ensure we are delivering the changes people around the country want."
