Pipers Row reopened after a final sweep by contractors after the major scheme to lay new track.
Track has been laid along Pipers Row as part of the extension planned from St Georges to Wolverhampton Railway Station.
It is hoped the West Midlands Metro passenger service will begin from 2020.
Which routes will be open?
Traffic will be able to enter or leave Pipers Row from Tower Street, Castle Street, Queen Street and Berry Street.
But vehicles accessing Pipers Row from the right-hand turn on Bilston Street will need to follow a diversion via St Georges Parade and Garrick Street before turning left into Pipers Row at Bilston Street.
The diversion will no longer go via Market Street.
The right-turn access from Bilston Street into Pipers Row will open again in October as work finishes on installing the traffic light system.
Bus services affected by the closure of Pipers Row will also return to the bus station.
Railway Drive will remain closed as work on third phase of the project continues.
Why is the work being done?
Councillor Roger Lawrence, leader of Wolverhampton council and portfolio holder for transport on the West Midlands Combined Authority, said: “The reopening of Pipers Row in time for the start of the school term is great news for Wolverhampton.
"This Metro extension has a key role to play in unlocking further investment and jobs, not just in Wolverhampton but across the Black Country.”
Laura Shoaf, managing director of Transport for West Midlands said: “This extension has reached a major milestone and the fact that we are already at such a key stage in the project is good news.
"When operational, the Metro extension will not only bring fantastic benefits to the city, but will play an important part in creating a transport network that helps bring greater prosperity to the West Midlands.”
New route closure in Birmingham from tomorrow
Commuters from the Black Country travelling to Birmingham are being urged to plan ahead and leave more time for their journeys as the next stage of the Westside Metro extension takes place.
The next stage will start tomorrow and will see Paradise Circus closed in both directions to facilitate the construction from Victoria Square to Centenary Square.
It will remain closed until summer 2019.
The A38 Queensway underpass, which runs beneath Paradise Circus, will remain open in both directions to allow access to and from the Aston Expressway and M6.
Centenary Square will close to vehicles from Monday, but will remain open to public transport until mid-September.