The plans will see the capacity increased to around 10,000, with new corporate boxes and a conference centre included in the redevelopment.
The £12million project put together by the football club and Northampton Borough Council will also see the area surrounding the stadium redeveloped, with additional planning applications for housing, local retail facilities and a hotel also to be submitted in the next few months.
"This is a momentous day for the club and our supporters," said Cobblers chairman David Cardoza.
"I will be honest, there were times when I never thought we would get here and without the fantastic support of David Mackintosh and Northampton Borough Council in the last couple of years we wouldn't have. But now the club can look forward to a very bright future.
"Now we have this approval we can really start pushing things on. Things are already moving forward quickly and it is possible that we will be building the roof and part of the structure of the new East Stand during the season and then finishing it off in the close season.
"We are working at a pace and the plan is to have the East Stand done by the start of next season, the hotel is going to take a little bit longer but hopefully we will be putting a planning application in for that in the next month or so.
"Our plans are also to give the West Stand an overhaul and to put new seating in to the North and South Stands. Sixfields will soon look very different and we will share our plans with supporters in more depth over the next few weeks.
"We can all be very excited about the future and so can our supporters. This is fantastic news."