In a rare consolation for President François Hollande's party, the Socialists held on to control of Paris, where Anne Hidalgo, 54, will become the first female mayor of the French capital after a victory that was far more comfortable than anyone had expected.
But Limoges, a town that had been run by the left for 102 years, fell to the UMP, as did Toulouse, the Champagne capital Reims and Saint-Étienne, as well as dozens of other smaller urban centres.
"It has been a black Sunday," said Socialist deputy Jean-Christophe Cambadelis.
Candidates backed by Marine Le Pen's FN secured the mayor's seat in the mid-sized southern towns of Beziers and Frejus and other smaller towns, adding to its first-round victory in the northern town of Henin-Beaumont.
"We have moved onto a new level," Le Pen claimed. "There is now a third major political force in our country."
"We have had a very severe warning," acknowledged Segolène Royal, Hollande's former partner who is tipped for a return to government in the reshuffle that is expected to follow in the wake of Sunday's rout.
The FN meanwhile faces a test of its ability to run the towns it has won. That has generally not been the case when the party has secured a handful of mayoral positions in the past.