The building now features a new Education Pavillion where people can learn more about the National Bard.
The cottage is a key part of the National Trust for Scotland's £21 million Robert Burns Birthplace Museum Project, which is due for completion next year and was the starting point for this year's Homecoming celebrations.
The First Minister re-opened the cottage and announced £2.1 million of additional support for the project, bringing total investment in the project by the Scottish Government to £7.6 million.
Burns Cottage was built in 1757 by Robert Burns' father, William Burnes. Scotland's national bard was born in the Alloway cottage on January 25, 1759. The 250th anniversary of Robert Burns' birth inspired Scotland's Homecoming 2009 celebrations which conclude on St Andrew's Day.
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The opening was part of the FM's programme of activity around the Homcoming finale and St Andrew's Weekend.
The FM said: "The re-opening of Burns' Cottage and the opening of the Education Pavilion marks an important step forward in the Robert Burns Museum Project, which aims to celebrate the life and work of Scotland's globally recognised cultural icon.
"I am delighted to announce that the Scottish Government is investing a further £2.1 million in the Museum project, bringing our total support to £7.6 million.
Chief Executive of the National Trust for Scotland, Kate Mavor added: "The cottage where Burns was born is one of Scotland's iconic heritage sites, and the Trust is privileged to have it in its care. Our team of experts in Alloway has restored it in a highly imaginative way to enhance visitors' knowledge, understanding and enjoyment of Burns and his early life.
"The approach we've taken at the cottage gives just a hint of how interactive and inspiring our finished museum will be."
(GK/BMcC)
