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The presenter celebrated the milestone on Friday’s episode (20 August) of the long-running game show, during which a chance collection of letters spelt the words “poo anally”.
Riley was seen attempting to suppress her laughter as the two words were displayed on the board behind her.
Fans of the series took to social media to laugh at the opportune moment.
One user shared a photo of Riley standing next to the board, accompanied by the caption: “What a way to commemorate 3000 shows eh.”
The mathematician responded to the tweet, joking: “Is there any other way?!”
Last month, viewers were left in hysterics after the word “megab****” was revealed as a point-scoring word on the game show.
Riley joined Countdown aged 22 in 2009, replacing mathematician Carol Vorderman.
The 35-year-old currently presents alongside wordsmith Suzie Dent and newcomer Anne Robinson, who joined the programme in June.
The former Weakest Link presenter took over hosting duties from Nick Hewer.
Robinson is the first female host of Channel 4’s longest running series.