Flitcroft played for the England U21s 10 times in 1993. He was also called up to Terry Venables’ get-together England squad in April 1995, but ultimately was never capped for the senior side.

In March 1996, he was signed by reigning Premier League Champions Blackburn Rovers for £3.5 million, but was sent off on his debut in a 3–0 defeat to Everton. Rovers were relegated to Division One in 1999 and new manager Graeme Souness appointed Flitcroft captain ahead of the 2000–01 season, in which Rovers gained promotion back to the Premier League. Flitcroft continued in his role as club captain for the next three years, but was suspended for Blackburn’s 2001-02 League Cup victory although he did lift the trophy with match captain Henning Berg.

On 23 March 2009, it was announced that Flitcroft would replace Lee Merricks as manager of Northern Premier League side Leigh Genesis. This also came with the news that the club had moved into their new ground at Leigh Sports Village. Flitcroft left Leigh Genesis after revealing to the media that he and many of his players had not been paid at Leigh for some time, and moved to Leigh’s rivals, Chorley F.C. in May 2010.

In September 2011, Flitcroft was named as a “core participant” in the Leveson Inquiry into the News International phone hacking scandal.

Flitcroft was hugely successful at Chorley, earning them two promotions – as Northern Premier League Division One play-off winners in 2010–11 and then Premier Division Champions in 2013–14. He immediately guided Chorley to 4th place in the Conference North but lost 3–2 at home to Guiseley in the Play Off Final. On 2 July 2015, Flitcroft stepped down as manager and his assistant Matt Jansen was put in charge. He is still at the club in a director’s role.