Alnwick started his career at Sunderland in 2004, having progressed through the club's youth ranks, but never fully established himself in the first team.

He switched permanently to Barnsley in July 2012, and made 12 appearances, but was deemed surplus to requirements in September 2013, and his contract was terminated by mutual consent.

His performances against Leicester City and West Ham United, the games that won Sunderland promotion to the Premier League and Championship win respectively, were impressive.

Despite impressing, particularly in Sunderland's 3–2 defeat to Tottenham Hotspur where he made a penalty save from Robbie Keane, Alnwick was dropped in favour of Kelvin Davis.

Just two days after the January 2007 transfer window had opened, Alnwick joined Tottenham Hotspur for a fee of £900,000 in a deal that could rise to £1.3 million and saw Márton Fülöp going the other way for £500,000.

[6] Alnwick made his league debut in an M69 Derby on 12 January, keeping a clean sheet as Leicester won 2–0 at the Walkers Stadium.

[7] He kept four clean sheets in eight league games, conceding six goals before suffering a thigh injury as Leicester were relegated from the Championship.

[15] Alnwick moved to Doncaster Rovers on 4 March 2011 and stayed until 9 April 2011 after their goalkeeper Neil Sullivan became injured.

[18] However, after the signings of Mike Pollitt and Christian Dibble, Alnwick's contract was terminated by mutual consent on 2 September 2013.

On the same day he left Peterborough, it was confirmed that Alnwick had moved to fellow Football League One side Bolton Wanderers on a free transfer to offer competition for Mark Howard.

[26] At the end of the 2017–18 season it was announced that Alnwick had been named the Bolton Wanderers Player of the Year by the club's supporters.

[27] Having played no games for Bolton for the first half of the 2019–20 season, Alnwick decided in December to mutually agree with the club to terminate his contract with immediate effect.

Still awaiting his debut, Alnwick was named in Stuart Pearce's first squad as England under-21 coach, alongside another uncapped goalkeeper, Joe Hart.