The European Banking Authority (EBA) is to be relocated from London to Paris after Brexit, while the European Medicines Agency (EMA) will move to Amsterdam.
Between them, the two key EU regulators currently employ around 1,000 people in Canary Wharf.
Ministers from the 27 other EU member countries voted at a meeting in Brussels on which cities should become the agencies' new homes.
European Council President Donald Tusk called the "real winner" from the relocation decisions the 27 states who will remain in the EU after Britain has left.
The French capital beat off stiff competition to win the key agency in a victory Paris will view as a boost to its bid to get banks to shift operations from London after the UK leaves the EU.
Announcing the decisions, Estonian deputy EU affairs minister Matti Maasikas said the votes for where to relocate both agencies ended in a tie and had to be decided by the drawing of lots.
Paris was tied with Dublin in the battle for the EBA, while Amsterdam received the same number of votes as Milan for the EMA relocation.
Mr Maasikas said: "It was a tight competition, and we needed to draw a lot on both cases."
Italian prime minister Paolo Gentiloni denounced the decision to award the EMA to Amsterdam by picking names out of a bowl.
A spokesperson for the Government said the UK would continue to work with both relocated agencies.
"As part of our new deep and special partnership, we want to ensure close collaboration on major science, research and technology initiatives continues.
"This, of course, includes with the EMA.
"Our commitment to ensuring patients' safe and timely access to medicines remains unchanged.
"We are also keen to build a new positive relationship with the European Banking Authority.
"London is a global financial hub, and we are determined to maintain the sound regulatory framework and global standards that underpin the City's leading position."