Simon Williams established his first gallery Startle in Holt in April 2023, before opening another in Thornham last year.
He was approached by Jarrolds three months ago due to the previous occupier, Norfolk Reclamation, relocating.
He said: “I was first persuaded by a friend of mine that opening a gallery in Norfolk would be a good idea.
“We took over the [Jarrolds] space in early September, so it has been a quick turnaround.
“I’ve wanted to come to Norwich and working with Jarrolds, with all of their history, is just sensational.
“Norwich as a city is a really cool, vibrant place and being part of that is really special.”
Startle features artists of international acclaim including Thierry Guetta – known as Mr Brainwash – who featured in Banksy’s documentary Exit Through the Gift Shop, and Emma Gibbons who previously worked with Damien Hirst.
Nods to Norfolk can be found all around the gallery including a Monopoly board with Norwich landmarks created exclusively for the gallery by printmaker Jayson Lilley, and pictures taken in Great Yarmouth and Sheringham by photographer Richard Heeps.
Mr Williams added: “Art is such a personal thing. We want people to come and explore.
“My whole ethos is making art accessible. I want people to walk into a gallery environment and feel comfortable.”
Startle’s opening event saw huge interest with more than 1,000 people booked up to attend.
The gallery, which can be found on the second floor of the department store, is now open.