It is thought around 20 roles could be at risk during a consultation as the two teams, which currently employ around 180 people, come together.
The unified £315m-a-year ad sales business will be called DMG Media Advertising.
It brings together the second and third biggest circulation print papers in the UK, after The Sun, and the world's biggest newspaper website, MailOnline.
However, responsibilities for ad sales will be divided between digital and print.
Clare Rush, previously the chief revenue officer of Mail Brands, will be chief revenue officer in charge of digital ad sales, joint partnerships and client relations.
Grant Woodthorpe, previously the managing director of commercial at Metro, will oversee investment in the print titles and supplements, as executive director, investment.
Rush will report to Martin Clarke, the publisher of MailOnline, and Woodthorpe will report to Kevin Beatty, the chief executive of DMG Media.
DMG Media previously united print and digital for the Mail titles under one chief revenue officer in 2015. The company played down suggestions that this was being reversed, pointing out Clarke had continued to oversee digital advertising after 2015.
Charlie Cox, a long-serving lieutentant within parent company DMGT, is expected to step down as managing director of Metro after four years but continue working on projects after previously overseeing the group’s interests in Teletext and radio.
There has been speculation that DMG Media might consider merging some editorial resources between freesheet Metro and the Daily Mail, The Mail on Sunday and MailOnline, but a source close to the company said that there were no plans at this time.
DMG Media’s decision to merge Metro’s ad sales with the Mail titles would appear to rule out a sale of the morning freesheet title.
There have been on-off rumours about a disposal for years, although the company dismissed that speculation last autumn.
Industry observers said DMG Media is keen to consolidate the Daily Mail and Metro to combat the possible threat from Trinity Mirror, which has been in talks for months about buying Northern & Shell, the owner of the Daily Express and Daily Star.
Beatty said: "This change is a further unification of the advertising offer across DMG Media’s brands, enabling us to better serve advertisers and their agencies.
"These changes will make the combined DMG Media Advertising team fitter, faster and stronger and will help us to take full advantage of our enormous scale, leading brands and rich data assets."
MailOnline’s ad revenues were £119m in its last financial year and grew 9% in the last quarter.
The combined print ad take of the enlarged ad sales unit was about £196m. The Mail brands brought in around £129m and Metro £68m for the same period.
They have been run as different business units within DMG Media until now and reported their financial results separately, although they did collaborate in some areas such as brand partnerships.
DMGT is under pressure to cut costs after spooking investors with a cautious outlook for its 2018 financial year.
The group reported underlying ad revenues rose 2% at DMG Media in the last quarter.
The Daily Mail has increased its market share and Metro has increased distribution but both print titles are battling long-term headwinds as ad revenues move online.
Dominic Williams, the chief investment officer of Mail Brands, and Melanie Danks, the chief client officer, will keep their roles under Rush in the new set-up, which begins in March.
One observer described the merger of the Mail titles and Metro as the biggest change in DMG Media’s advertising operations in a decade since the Daily Mail and The Mail on Sunday teams merged.
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