Sixfields Tavern became engulfed in flames at about 14:30 GMT on Saturday afternoon.
Eighty firefighters worked for five hours to contain the fire and no-one was hurt.
Minor demolition work is to be carried out, as police and firefighters assess the damaged site.
Barry Mullan, incident commander, said: "The local employees did a great job in getting everyone out."
He said the fire began in a rear compound which contains a bin store and walk-in freezer, although the exact cause is not yet known.
Firefighters remain at the site watching for hotspots, which may reignite as the unstable areas are demolished.
The pub is at Sixfields Leisure, a site of shops, restaurants, fast food outlets and a cinema just yards from Sixfields Stadium, the home of Northampton Town.
Flames and billowing smoke could be seen above the stands as The Cobblers defeated Northwich 3-2 in the FA Cup on Saturday afternoon.
Lewis Dunnachine, who was in the pub, said: "We were finishing off our lunch prior to going to the Northampton Town match when I spotted spotted black smoke before the fire alarm went off.
"Our seats at the game enabled us to watch the building burn to the ground."
The game was unaffected and police assisted as supporters left the ground at full-time.
At the blaze's peak, firefighters were supported by crews from Oxfordshire and Buckinghamshire.
The operation was scaled down after 18:00 GMT.
A smell of burning lingers in the area where this time yesterday, Sixfields Tavern was a busy restaurant and pub.
It's now a carcass, burnt beyond all recognition. Part of the front of the building is still standing but from what I can see through the broken windows the inside is damaged beyond all reasonable repair.
It's a sad sight. This was a popular local and the pub of home fans on match day.
Police advised people to avoid the area on Saturday night and said Weedon Road roundabout remained closed on Sunday.
A Hungry Horse spokesperson said: "The pub will not be open for the foreseeable future and we will be working with the emergency services to establish the cause."
They added: "We sincerely apologise to our customers who have Christmas bookings with us, and will be contacting those whose telephone numbers we have as soon as we can to help them re-arrange their bookings, or where necessary, offer a refund of their deposits."
The venue was fully-booked for Christmas Day lunch.
James Stirling and Brian Miller were working at the pub when the fire took hold.
They described it as heartbreaking.
"I've already cried," said Mr Miller.
It is understood pub workers have been unable to collect their cars from the car park because their personal belongings, including keys, were in the staff room.
Staff at a fire-wrecked pub in Northampton have been praised by a fire officer for their quick actions in helping customers to safety.