From the earliest days of Milton Keynes as a new town, officially designated in 1967, plans were already being considered for a major stadium capable of hosting a top-level football team. The Milton Keynes Development Corporation, which oversaw the town’s development between 1967 and 1992, had identified the need for such a facility.

The stadium that would eventually become Stadium:MK was first proposed in 2000 by the Milton Keynes Stadium Consortium, led by Pete Winkelman and his company, Inter MK Group. The ambitious development included plans for a 30,000-capacity football stadium alongside a 150,000-square-foot Asda hypermarket, an IKEA store, a hotel, conference facilities and a retail park.

As part of the development, Asda paid Inter MK £35 million for its portion of the site, while IKEA contributed a further £24 million. Construction of the stadium began in February 2005. Later that year, MK Dons set an ambitious target of moving into the new stadium by January 2007.

By February 2007, the plans had been revised. The stadium was to open with an initial capacity of 22,000, with the ability to expand to 32,000 in the future. This replaced the original proposal for a 30,000-seat stadium.

Stadium:MK hosted its first match in July 2007, when MK Dons faced a Chelsea XI and recorded an entertaining 4–3 victory. Later that month, an England Legends XI played a World Legends XI in a memorial match for former England international Alan Ball.

The MK Dons played their first competitive league fixture at the new stadium on 11 August 2007, suffering a 2–1 defeat to Bury in front of 7,740 supporters. Four months later, on 29 November 2007, the stadium was officially opened by Queen Elizabeth II.

The stadium was designed by Populous, one of the world's leading architectural firms specialising in sports venues, arenas and convention centres. The company has been involved in the design of some of the world's most prominent sporting venues, including Arsenal’s Emirates Stadium, Wembley Stadium in partnership with Foster + Partners, Benfica’s Estádio da Luz, the expansion of the City of Manchester Stadium and the stadiums of Tottenham Hotspur and Queens Park Rangers.

Stadium:MK currently features two tiers and has a capacity of 30,500. Its distinctive high roof was designed with future expansion in mind, with the potential to increase capacity to around 45,000 through the addition of a third tier. The stadium was designed to meet UEFA’s Elite Stadium specifications and features a Desso GrassMaster playing surface.

Over the years, Stadium:MK has hosted a wide variety of sporting events. The venue has staged several England Under-21 internationals and was the setting for the 2015 Women’s FA Cup Final between Arsenal and Everton.

Rugby union has also featured prominently at the stadium. The first rugby match took place in May 2008, when Saracens hosted Bristol in Milton Keynes while Watford required Vicarage Road for their Championship play-off commitments. Northampton Saints later used Stadium:MK for their Heineken Cup quarter-final and semi-final matches in 2011, as their home ground was considered too small for major European fixtures.

The stadium was also selected as one of the venues for the 2015 Rugby World Cup, hosting three matches. One of these, Fiji versus Uruguay, attracted 30,048 spectators and established a new attendance record for the stadium at the time.

The South Stand is traditionally known as the “Cowshed”, a reference to Milton Keynes’ famous Concrete Cows. The nickname was inherited from the home supporters’ end at the National Hockey Stadium, the previous home of the MK Dons.

The North Stand is used by away supporters and is known by Dons supporters as the “Boycott End”. The name refers to the boycott organised by AFC Wimbledon supporters for the first competitive meeting between the two clubs. Despite the boycott, more than 3,000 AFC Wimbledon fans attended the match, a figure roughly equivalent to their average home attendance at the time.

The two side stands are simply referred to as the East and West Stands, reflecting their positions alongside the pitch.

The Stadium:MK complex also includes the Marshall Arena, a 3,420-square-metre multi-purpose events venue spread across three floors. The arena is used for a wide range of events, including music performances, sporting competitions, conferences, exhibitions and private functions. It officially opened on 8 February 2014, hosting the English National Badminton Championships as its first major event.