Starting with Arsenal, and later playing for Oxford United, Brian McDermott joined Exeter City as the club was building towards winning Division Four in 1990. Playing an important part in the Grecians championship success, Brian later served in a number of roles for Reading before later managing the Berkshire club as well as Leeds United.    

Having earlier been on associated schoolboy forms with Queen's Park Rangers, Brian joined Arsenal as an apprentice in 1977 after being spotted playing for Slough schools. He signed professional forms in February 1979 and was a regular scorer for the reserves prior to making his first-team debut as a substitute against Bristol City in March 1979. Brian featured regularly for Arsenal’s first-team during both the 1980/81 and 1981/82 seasons although he appeared less-frequently in 1982/83 and 1983/84. 

Following loans to Fulham and IFK Norrköping (where he enjoyed great success) Brian secured a permanent move to Oxford United in December 1984 having made around sixty league appearances for Arsenal whilst scoring a dozen times. He went on to play 24 league matches for Oxford, scoring twice, also spending time on loan with Huddersfield Town. He then moved to Cardiff City in August 1987 where he remained until his transfer to Exeter City in February 1989. 

Initially arriving at St James’ Park on loan, Brian soon joined the club permanently once a £7,000 fee was agreed for his services. First appearing against Burnley 18 February 1989, Brian appeared in the final nineteen matches of 1988/89 scoring once. Then, with 38 league starts (with another three appearances from the bench) Brian - often wearing the number nine shirt  but playing on the wing - became a key member of the club’s Fourth Division championship winning team in 1989/90. Remembered as a fast, clever played who could use a body swerve to great effect Brian's goals in that memorable campaign came agaist Hereford United, Southend United - when he scored the winner on the night City won promotion - and Lincoln City.

Yet Brian’s days with the Grecians were numbered and in November 1990, after only another eight league games, he signed for Conference side Yeovil Town for a fee of £10,000 where he became assistant player-manager and made over sixty appearances before retiring from playing. In time, after management positions at Slough Town and Woking, Brian joined Reading as chief scout in September 2000 and went on to become the club’s  under-19 and reserve team manager.

Taking over as caretaker first-team manager following the departure of Brendan Rodgers in December 2009, Brian was an immediate success and soon signed a 12 month rolling-contract to become Reading's full-time manager. Having already led the club to an unsuccessful Championship playoff final, Brian steered Reading to the Premier League by winning the Championship in 2012. With the club facing an immediate relegation the following season Brian was sacked in March 2013. He then swiftly returned to management at Leeds United before serving again as Reading manager in 2015/16.

Thereafter Brian worked as a scout for Arsenal and as a consultant for the League Managers' Association ahead of, in May 2023, his appointment as director of football at Hibernian.