Passengers were faced with longer journeys over the past five months as engineers worked round-the-clock to renew 1,800m of concrete slab track and install more than 4,000m of new rails through the structure.
High-level services were originally due to restart on Monday but ScotRail announced last month the tunnel will open a day earlier, with normal services resuming on Sunday.
Station platforms and track layouts within Queen Street have also been extended and altered as part of the project, and both the tunnel and station have been prepared for the electrification of the main Glasgow-Edinburgh line next year.
Transport minister Humza Yousaf helped tighten the final bolts on the new slab-track inside the tunnel on Friday.
He said: “This has been an unprecedented project, both in engineering terms and in the scale of the operation required to keep people moving and services diverted via the underground platforms during the works.
“This is a key milestone in our programme of investment for Scotland’s railways and literally paves the way for the introduction of a new generation of electric trains.”
Phil Verster, managing director of the ScotRail Alliance, said: “The successful, early delivery of this project will allow us to introduce faster, longer and greener trains on the main Edinburgh-Glasgow line - delivering thousands of extra seats, shorter journey times and improved accessibility for customers.”
Over the next three years, works will continue within Glasgow Queen Street as engineers extend the station out towards George Square and create a new concourse and passenger facilities.