The track opened in 1969 as a combined horse and auto racing facility under the control of David P. Buckson, then-Attorney General of Delaware.

The description of Miles the Monster has drawn comparisons by Roadside America to The Thing and the Hulk, and was inspired by the "theme of concrete" according to Joe Heller, a former DMS PR worker.

[12] The plan received mostly positive reception from the Delaware General Assembly, with local lawmakers favoring changing laws in order to legally build the track.

201 was passed through both branches of the General Assembly on July 18[15] and signed into law by Delaware Governor Charles L. Terry Jr. eight days later.

[21] By April, construction completion was moved to August,[22] and in June, multiple liens totaling at least $286,500 were filed against Dover Downs.

In April 1970, McNutt Electric Company, one of the lienholders, sued Dover Downs for unpaid bills.

In 1973, it faced a near-boycott by the Cloverleaf Standardbred Owners Association, who demanded an 8% purse increase and new paddock facilities.

[48] Despite DDR's issues, DDIS remained profitable, with The Morning News noting that auto racing was unaffected by the complex's financial troubles.

[49][50] In 1975, a tax break bill passed to assist Dover Downs if it resumed thoroughbred racing, easing some financial pressure.

[51][52] However, a year later, auditors found Dover Downs owed $49,000 (adjusted for inflation, $262,365) in unpaid admission taxes.

[56] Du Pont agreed to sign it only if he could release Dover Downs' financial records, which the track’s owner, Riddle, had previously refused.

[57] In a controversial decision, du Pont approved the $500,000 (adjusted for inflation, $2,335,714) annual tax break on February 21.

[60] Riddle maintained that he thought the track was in a stable financial state, proclaiming that "I really believe that this racetrack is solid and will continue to be so for many years".

[61] However, owner John W. Rollins said he hadn’t made a profit on the track, noting his financial support had kept it afloat.

[62] In November 1979, director of operations Denis McGlynn was named as Riddle's replacement for president of Dover Downs.

[63] Heading into the 1980s, the facility experienced continued financial woes, with McGlynn reporting "significant" losses since 1981 in a March 1983 interview.

[66] In April 1983, McGlynn tried to negotiate with the city to lower the buying cost of Dover Downs to $1.9 million; however, the proposal was rejected.

[69] Later that year in May, in response to rising attendance and subsequent complaints about a lack of seating at DDIS, McGlynn announced a long-term expansion plan to retain its NASCAR races.

[85] In contrast, Dover Downs Raceway, alongside the state of Delawarean horse racing, oversaw heavy turmoil in the late 1980s and most of the 1990s.

[89] Five years later, despite threats of another veto from Castle's successor Tom Carper,[90] another push for legalization was made in early 1994 after the closure of Brandywine Raceway in 1990 and further economic turmoil due to H.B.

[103][104] By November 1996, $800,000 worth of renovations were invested into a reinvigorated and financially stable DDR, with McGlynn praising Rollins in a News Journal interview.

The first phase of the project was completed in time for the 2007 Autism Speaks 400, with additional parking and luxury seating options being constructed.

[120] Phase two was completed by the running of the 2008 Camping World RV 400, which included the construction of a monument honoring past winners at DIS alongside an expanded fan zone.

[11][121] Phase three of the project, an extension of the track's pit road, was completed by the 2009 Autism Speaks 400, extending it by 432 feet (132 m).

[135] As of 2024, DMS holds one annual NASCAR weekend, currently known as the Autotrader EchoPark Automotive 400 for sponsorship reasons.

[147][148] However, after one more iteration in 1999,[149] the race was scrapped heading into the new millennium, with poor attendance being cited as the main reason for the failure to renew.