Estate agents, new homes and overseas developers will be able to upload their properties directly on to the site, with firms such as Connells, David Wilson Homes and Mayfair International already signed up.
The new overseas section will complement the newspaper supplement launched earlier this year.
The additions follow the launch of the website's dedicated property search engine, powered by Gabriels Technology, in May.
The site also includes historical house price reports for every home sold in the UK since 2000.
Telegraph.co.uk travel product manager Janet Irwin said: "The battle for online traffic means that all sites have to keep themselves up to date. The Telegraph has taken a phased approach in developing the property site and has a very long-term development plan."
She added that the site's revenue streams currently come from banner ads although there were plans to charge firms to advertise their properties online in the future.
The Telegraph is due to launch a new property section for the North of England this week, which will also be available online.
Other recent online developments at telegraph.co.uk include a new search engine to its travel section, allowing users to find holiday deals across a range of new travel businesses, such as Thomas Cook and Cosmos.
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