As well as the previously-announced Cabinet Office headquarters in Glasgow, the extra Foreign Office jobs will move to the South Lanarkshire site.
It means more than 1,000 UK civil service jobs are due to be relocated to Scotland in total in coming years.
Cabinet Office Minister Michael Gove said the move would “co-locate the engine room of the UK Government in Scotland”.
Foreign secretary Dominic Raab said the relocated jobs would ensure the civil service “represents all parts of the UK”.
The 500 additional roles will bring the Foreign Office’s staff in East Kilbride to 1,500 by 2025.
The announcements come as the Scottish Conservatives hold their virtual spring conference ahead of Holyrood elections in May.
Mr Gove said: “The Cabinet Office’s new HQ in Glasgow will co-locate the engine room of the UK Government in Scotland, bringing decision makers closer to the communities they serve and ensuring closer collaboration between Scotland’s two governments as we tackle the Covid-19 pandemic together and work to build a sustainable recovery.
“Not only will this bring new jobs and investment to Scotland, it will strengthen the diversity of the UK civil service, ending the Westminster-knows-best approach to policy making and ensuring Scottish voices shape everything we do.”
Mr Raab added: “There can be no clearer demonstration of commitment to our joint HQ in East Kilbride than today’s announcement that an extra 500 Foreign, Commonwealth and Development Office jobs are coming to Scotland. This will further ensure the civil service represents all parts of the UK and will be a boost to the Scottish economy.
“Staff at Abercrombie House are at the forefront of delivering the UK’s diplomatic clout, as we prepare to host the G7 and COP26, while supporting the delivery of our £10 billion aid budget to continue helping the world’s poorest people.”
The East Kilbride building was previously home to the Department for International Development (Dfid) before it was merged into the Foreign Office.
SNP MSP George Adam said: “Since 2010, the Tories have axed 7,000 civil service jobs in Scotland.
“In a period of Westminster austerity, the UK Government chose to disproportionately slash jobs north of the border – today’s announcement is a drop in the ocean.”