The theatre is among more than 2,700 recipients to benefit from the latest round of awards from the £1.57 billion fund.
This award will go towards a "safe and sustainable" reopening of the Gatehouse Theatre after pandemic restrictions are lifted.
More than £300 million has been awarded to thousands of cultural organisations across the country, including Stafford Gatehouse Theatre, in the latest round of support from the Culture Recovery Fund.
Over £800 million in grants and loans has already been awarded to support almost 3,800 cinemas, performance venues, museums, heritage sites and other cultural organisations dealing with the immediate challenges of the coronavirus pandemic.
The second round of awards made will help organisations to look ahead to the spring and summer and plan for reopening and recovery.
A spokesman for the Gatehouse said: “The Gatehouse Theatre has long been part of the Staffordshire arts scene, and is proud of its heritage in supporting both the arts and the community.
"While the past year and the pandemic restrictions have taken a toll, the theatre is looking forward to re-opening with a brand new look and a great season of shows. We are so grateful for the support of our staff, volunteers, audiences, and the public over this time.”
The funding awarded is from a £400 million pot which was held back last year to ensure the Culture Recovery Fund could continue to help organisations in need as the public health picture changed. The funding has been awarded by Arts Council England, as well as Historic England and National Lottery Heritage Fund and the British Film Institute.