A sharp decline towards the end of the era saw Derby lose their status as full league members for the only time in their history with relegation to the Third Division North in 1955 before they returned at settled in the Second Tier for much of the next 15 years.

Adopting a kit of amber, chocolate and blue, the club began to aggressively gather players, including Derby Midland's star winger George Bakewell and Darley Abbey's Ernest Hickinbottom, and embarked on an extensive programme of friendlies, beginning with a 6–0 away defeat by Great Lever on 13 September 1884.

There was also controversy in the FA Cup, when the 1st round tie against Sheffield Wednesday was declared void not once, (a 2–3 defeat) but twice (a 1–0 win) when the losing club on each occasion successfully questioned the eligibility of an opposition player.

Derby started the new century with a sixth-place finish and appointed its first full-time manager in Harry Newbould, the first time a single man was in sole control of first team affairs.

"Men argued with each other in pubs up and down England, not about the menace of the Kaiser's steel-helmeted hordes but about the price paid to Derby County for Horace Barnes" After the breakout of World War I, the football authorities decided to carry on with the league programme despite criticisms it was unpatriotic.

During this five-year break, Derby played one season in the wartime Midlands Section during 1915–16, before closing down for the duration of the war, the majority of the club's players turning out for Notts County.

Despite rumours linking former-England International Colin Veitch with the position, the club announced on 4 July 1922 that, after interviewing four applicants for the job, they had appointed Cecil Potter.

He instead, however, replaced Herbert Chapman at Huddersfield Town, who had been lured away by Arsenal and won the league title, completing English Football's first ever Championship Hat-Trick in the process.

Jobey always displayed a hunger for talented centre forwards, and the key signing was England International Harry Bedford, at a cost of £3,250, from Blackpool, who scored 27 goals as the Rams finished runners up to Sheffield Wednesday in the 1925–26 Second Division table.

Despite scoring 90 goals, 30 of which came from Harry Bedford – equalling the club record set by Alf Bentley 20 years before – they conceded 82, and had to settle for the runners-up spot.

In January and February he equalled the club record of scoring in six consecutive games, hitting 15, though Derby's now customary shaky defending saw them still manage to lose three of them.

Although the first team could only finish second, the reserves, boosted by the presence of Jack Bowers who hit 30 goals as his slow recovery from the knee injury suffered in 1934 continued, won the club the Central League Championship for the first time.

With Hughie Gallacher sold to Notts County for £2,000 (after hitting 38 goals in just 51 games) Jobey reinforced his side for the 1936–37 season with the capture of Aston Villa strikers Ronnie Dix and Welsh international Dai Astley.

Derby where offered a place in a substitute competition but, mindful of criticism of being unpatriotic after continuing on following the outbreak of World War I, tested the water with a friendly against Leeds United.

At the time the maximum wage system was still in place, and was not to be successfully challenged for another 20 years, and the commission, which was, curiously, acting on allegations forwarded by Jobey, who supplied details in support of them, found that 'various payments in excess of those allowed under the transfer, bonus and signing on regulations of the Football League have been made by the Derby County club over a period of 12 seasons.'

With the addition of these two, and the appointment in Match 1945 of Ted Magner, the first official successor to George Jobey, Derby won the double of the 1944–45 Football League North (Second Session) and the Midland Cup, beating Aston Villa 9–0 on aggregate.

As no guests were allowed in the 1945–46 FA Cup campaign Magner had to act quick to secure the signatures of Doherty and Carter, acquiring them for £6,000 each from Manchester City and Sunderland respectively.

The format of the 1945/46 FA Cup meant Derby's first ever appearance at Wembley after playing a total of 10 matches and scoring 33 goals, including 12 from Sammy Crooks and 10 from Peter Doherty.

Derby finished the season, mid-table, in 14th, but chairman Ben Robshaw was determined for the Rams to maintain the success of the 1930s and sanctioned McMillan to break the English transfer record with the £15,500 capture of Billy Steel from Greenock Morton.

This led to an investigation by the Football League auditors who summoned another joint commission with the FA, mainly focused on accusations of payment of excessive wages, as it had under Jobey's reign, concerning a Czechoslovakian tour undertaken by the, then, cup holders.

Jack Lee, who had joined from Leicester in June, finished the season as top scorer with 28 goals, including four in a 6–5 victory over Sunderland in December, and played and scored for England in a 4–1 win over Northern Ireland at Windsor Park.

However, Dunn was soon ruled out for the rest of the campaign after a cartilage operation and the club only recorded 4 victories in the next 20 matches, a run which included 10 without a win, eventually finishing bottom.

Attendances dropped to an average of just 15,000, the lowest since the 1920s, and, with the close season departure to Boston United of Reg Harrison, the last of the FA Cup winning side at the club, went any connection with the Golden age of the 1930s and 1940s.

The club reacted to relegation in 1954–55 by sacking Jack Barker, whose 19 months in charge at the Baseball Ground left him very bitter: "I wouldn't be a manager again for £10,000 a week.

Making it his priority to establish leadership and discipline on the field, as well as off it, Storer made the inspirational capture of FA Cup-winner Reg Ryan for just £3,000 from West Bromwich Albion.

The style and success of Storer's attacking football saw the club regularly gather 20,000 home gates for the first time since relegation from the First Division, and even attracted 29,886 for the visit of Chesterfield in April 1957, a match in which they recorded their biggest win of the season with a 7–1 victory.

Storer bought in Bill Curry from Brighton and Hove Albion for £12,000 in the 1960–61 season in an attempt to bring an extra flourish to the stagnating Rams team.

Barrowcliffe went on to make his 500th appearance for the club when he started the 2–1 away defeat by Carlisle United on 7 September, only the fourth player to do so after Jimmy Methven, Steve Bloomer and his teammate Jack Parry.

The gradual improvement under Ward seemed to free the wallet of the board and, ahead of the 1966–67 season, broke the club transfer record with the £40,000 signing of Kevin Hector from Bradford Park Avenue, where he had hit 113 goals in just 176 games.

Ward's five years at Derby were blighted by a lack of cash and a parochial attitude of the boardroom, but he is often credited with laying the foundations for the success of the 1970s, thanks to the signings of Hector and Durban, as well as providing first team football for Ron Webster, Colin Boulton and Peter Daniel, all of whom were part of the club's later title winning sides.