Easyjet or Loganair already fly most of the routes, or to Belfast International.
They are among 23 routes across the UK announced on Tuesday that will start to be launched from Wednesday, April 13 – days before Easter – by new owner Thyme Opco, which is linked to US hedge fund Cyrus Capital.
Flybe went into administration in March 2020, with the onset of the Covid pandemic seen as the final straw for the ailing airline, which had struggled with high operating costs.
The carrier, whose headquarters has been switched from Exeter to Birmingham, previously had the most routes within the UK.
Its re-emergence is likely to be met with fierce competition from Easyjet and Glasgow-based Loganair.
The latter took over many of Flybe's Scottish routes and now describes itself as flying to more UK destinations than any other airline.
Loganair also previously beat off rival flights launched by Flybe and its partners Eastern Airways to the Western and Northern Isles.
Glasgow-Belfast City will be the first new Flybe route to serve Scotland, up to four times a day from April 14.
The others do not start until the summer, with up to three flights a day between Edinburgh and Belfast City from June 23.
The Edinburgh and Glasgow links to Birmingham both launch on July 28, with up to four flights a day from the capital and up to three a day from Glasgow.
Daily flights from Aberdeen to Birmingham begin on August 18, and to Belfast City up to four times a week on August 25.
Inverness-Belfast City flights up to four times a week start on August 25.
Flybe chief executive Dave Pflieger said: "We are delighted to now be out for sale and starting service next month.
"We think our new flights will benefit everyone who wants low fares and more flights to go on holiday and visit loved ones.
"Our new network will also ensure better regional connectivity inside the UK and between various UK and EU regions.”
Matt Hazelwood, chief commercial officer of AGS Airports, which owns and operates Aberdeen and Glasgow airports, said: “The re-emergence of Flybe as an airline is welcome news for the industry and our passengers as we continue to rebuild the vital connectivity Scotland relies on.
“Both Birmingham and Belfast are important destinations for us, so these additional flights to the UK’s second largest city and Northern Ireland’s capital will offer even more choice and convenience for our customers.”
Graeme Bell, general manager at Inverness Airport, said: “We are pleased that Flybe will once again be operating flights from UK regional airports, including Inverness.
"As we continue the recovery from the worst of the Covid pandemic, we welcome the introduction of additional choice for passengers.”
Kate Sherry, aviation director at Edinburgh Airport, said: “It’s great to see the Flybe brand fly back to being a feature of UK airports.
“They’ll play a big part in offering more choice to travellers and getting the UK’s connectivity back to where it should be."