The 84 glass-fibre GoGoDragons! - all 5ft (1.6m) tall and which were part of a community art trail - were sold at The Forum in the city.
The auction raised £369,500 for charity Break, which cares for vulnerable people.
The dragons were painted by a variety of artists and in many styles.
One painted by 12-year-old art prodigy Kieron Williamson sold for £20,000, while a glittering mosaic dragon went for £25,000.
Dragons feature in much of Norwich's architecture and the city has churches dedicated to Saint George in Tombland and Colegate - both of which house dragon symbols.
The event follows on from 2013's GoGoGorillas! trail, which raised about £270,000 for charity at auction.
Hundreds of thousands of pounds have been raised for charity by the sale of dragons that have been on display in Norwich.