The appointment of Ad 2-one marks the first time the site has worked with a sales house.
Rightmove is consistently ranked among the UK's top 10 largest sites, according to research company Hitwise. Of the top four property websites, the site has 85% market share by pages viewed, and more than 80% of all UK estate agents choose to list all of their properties on the site, according to Hitwise.
The site claims it has 18 million visits from active home movers and more than 450 million page views every month.
The advertising will appear on a new part of the site that will provide local information.
Ad 2-one account director Jo Pike said: "Historically, advertising was not allowed on the site. The advertising will not just appear on the run of the site but we will be launching with advertising on the local information pages."
Pike added that advertisers would be able to target using information gathered by people going through the house-moving process on the site.
Other Ad 2-one clients include the majority of IPC's magazine portfolio, Lonely Planet, the Discovery Channel and Eurosport.