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The 49-year-old took his press duties as normal around 1pm today ahead of the fixture with Southend.
However, within hours he was dismissed after a board meeting headed by chairman Iain McInnes and chief executive Mark Catlin.
Backroom staff Steve Allen, David Connolly, Dave Coles, Alan McLoughlin and Andy Awford were later called to Fratton Park when the news was delivered to staff.
Whittingham has paid the price after four successive defeats saw the Blues knocked out of two cup competitions and slip to 18th in the table.
Saturday’s 2-1 home loss to Scunthorpe was met with boos and chants of ‘That was embarrassing’ from the Fratton faithful.
Former fan favourite Whittingham took over at Fratton Park last November but managed only 11 wins in 51 games.
The club currently lie 18th in the League Two table having lost their last three league matches, including a 2-1 home defeat at the hands of Scunthorpe United on Saturday.
A statement on the club's official website said: 'Portsmouth Community Football Club regret to announce that, following a meeting with the chairman, CEO and finance director, Guy Whittingham has today left his post as manager after his contract was terminated
'The club wishes to place on record its sincere gratitude to Guy for his service to the club during difficult times.'
Whittingham took over as caretaker manager at Fratton Park in November 2012 following Michael Appleton's departure to Blackpool before being appointed the club's permanent manager in April of this year.
The 49-year-old scored 99 goals in 173 appearances during his playing days with the south coast club, including a record of 42 goals in the 1992/93 season as Pompey missed out on automatic promotion to the Premier League on goals scored.
An early favourite for the South Coast job is former Gillingham boss Martin Allen.
In the meantime, academy boss Andy Awford will take caretaker charge for Tuesday's home clash with Southend and will be assisted by first-team coach Alan McLoughlin and striker David Connolly