The Ministry of Housing, Communities and Local Government is setting up the first ever ministerial office outside of London in the city under plans revealed last month.
Senior members of Wolverhampton Council are now having meetings with the Government to discuss where the new office will be.
Among the properties being considered is the i9 building in the city centre, where construction is continuing after the completion of the i10 complex opposite and the nearby £150 million railway interchange.
However no final decision has been made, with talks set to take place between local and national government bosses this week.
Wolverhampton Council’s director of regeneration Richard Lawrence said: “People will be aware of the recent announcement by the Ministry of Housing, Communities and Local Government about their first headquarters outside London.
“We are working with them and have a meeting this week to discuss their requirements and a suitable location.
“These are all positive things that are happening around the station interchange.
“While we have been through a lockdown period, all these investment enquiries have progressed and I think we are seeing this as testament to what has been happening around the i9 offices.”
Mr Lawrence said the i9 building was due to be completed in the next few months.
“Quite a lot has happened [in Wolverhampton] during the lockdown period and I want people to see what has been achieved,” he said.
“Adjacent to the multi-award-winning interchange railway station project is the i9 building as part of the commercial district, which is pretty much fully built and is awaiting completion by the summer time.
“We are in legal talks and hoping to let very shortly to at least two organisations and are confident that we will have the building open and fully pre-let by summer time this year."
Government staff are being relocated across the UK under the Places for Growth programme aimed at moving away from a fully London-centric approach to government.
Around 500 posts, including senior civil servants, are due to be based in the West Midlands by 2025 with many of these set to be in Wolverhampton.
The housing department, which is headed by former Wolverhampton Grammar School student Robert Jenrick, will keep its London office but have a dual office in Wolerhampton.
Mr Jencirk, the communities secretary, said a "regular ministerial presence" was to be expected in the city.