The first league game took place at Millmoor and Rotherham County beat Nottingham Forest 2–0 but it proved to be a season of struggle and they finished in 17th position out of 22.
When it was decided to introduce Division Three, Town were hopeful of becoming Rotherham's second League club but they received just 13 votes, not enough to gain admittance.
After adopting Arsenal-style white sleeved shirts, United finished as runners-up three time in succession between 1947 and 1949 and then were champions of Division Three (North) in 1951.
Not only did the Millers pip one of their neighbours, Barnsley, to the championship but the double they recorded over Sheffield United helped send them tumbling into the fourth division.
This team, which included the attacking talents of John Seasman, Tony Towner, Rodney Fern and Ronnie Moore could not maintain this level of performance, however, although it was something of a surprise to see them relegated again the very next year.
The problem was compounded as Rotherham had already sold their ground to Ken Booth in return for clearing £3 million of debt and had no tangible assets, so administration was not a viable option.
An eleventh-hour intervention by a consortium of local businessmen offering substantial investment and a new business plan averted a possible dissolution of the club.
Rotherham United began their second successive year in League One with a 10-point deficit as a result of the CVA which saved the club from liquidation.
At one point during the close season, the team had only seven full-time professionals on the books but Knill made a number of signings during this period to bolster the squad including former Liverpool winger Richie Partridge, ex-Premiership players Delroy Facey and Martin Woods, former Bayern Munich and Nottingham Forest star Eugen Bopp and many others who have played at a higher level.
At the arrival of the January transfer window, Knill sold stars Lee Williamson and Will Hoskins to Premiership side Watford for a combined fee in the ranges of £1.2 million.
The Millers spent the majority of the 2007–08 season in the automatic promotion places, winning eight consecutive league matches towards the end of the year.
This led to further complications after the Football League demanded a £750,000 bond for the team to play outside of the Town's boundaries for a maximum of four years.
[13] Under the new ownership of Tony Stewart, Rotherham won their first game of the 2008–09 season at the Don Valley stadium with a 1–0 win against Lincoln City.
This included victories over higher league opposition in the form of Wolverhampton Wanderers, Southampton, Sheffield Wednesday, Leicester City and Leeds United.
Despite losing top scorer Reuben Reid to West Bromwich Albion, Mark Robins kept the majority of the team together from the 2008–09 campaign whilst bolstering his squad with the signings of Tom Pope, Adam Le Fondre, Nicky Law, Jamie Annerson, Paul Warne, Andy Liddell and Kevin Ellison.
The Millers continued their good run of form into the season, winning 3 of their first 4 games, before beating Derby County in the cup.
The next week saw the Millers close to completing another giant killing narrowly losing 4–3 to West Brom after extra time and being knocked out of the Football League Trophy at the hands of Huddersfield Town.
[14] Assistant manager John Breckin took charge of the team overseeing their 3–1 win over Chesterfield, moving the Millers to top of the league.
An announcement was set to be made at 2.15 pm on Monday 7 September to unveil Robins as the new manager of Barnsley, however talks stalled due to a disagreement over compensation.
[15] Mark finally left the millers on Wednesday 9 September, having signed a contract with Barnsley the previous evening, leaving Steve Thornber in temporary charge.
[18] In the final against Leyton Orient, the game went to a penalty shoot-out, where two saves from Adam Collin secured a second successive promotion for the club.
[19] In the 2014–15 Championship season, Rotherham's first after a nine-year absence, their survival was jeopardised by a points deduction for fielding the ineligible Farrend Rawson during their home win against Brighton & Hove Albion, Farrend Rawson's loan had expired two days prior to the match, and despite the club insisting it was an external administrative error, they were subsequently thrown back into a relegation battle with Wigan Athletic and Millwall.
[21] Rotherham sold key players from their promotion winning campaigns before the 2015–16 season, including Ben Pringle, Craig Morgan and Kari Arnason.
Evans left the club in September[22] and former Leeds United manager Neil Redfearn was appointed as his replacement,[23] being sacked in February 2016 after a run of six defeats in eight games.
[37] Early in the 2022–23 season, manager Paul Warne departed for Derby County,[38] being replaced by Exeter City boss Matt Taylor.