The Office of the e-Envoy has accepted demands from the Welsh Language Board that its websites should be bilingual.
Whitehall's web design handbook has been changed so that each site will have the option to been displayed in Welsh or English.
The requirement is a key part of evidence given by the Welsh Language Board in a consultation exercise in 2001.
Board chairman Rhodri Williams said: "This is excellent news both for the board and for the language itself."
Statutory organisations operating in Wales will now have to consider the two languages when developing their sites on the internet.
The Government's handbook now demands that "Welsh content should be as easy for the public to access as English content", and points to the Welsh Assembly and Welsh Language Board as examples of bilingual sites.
In fear of future shortage - or in preparation for its own electric car project?
New Spectre microcode patches released by Intel to fix security flaws in Skylake, Kaby Lake and Coffee Lake CPUs
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Malware has been in circulation for more than a year