Brook began his football career, as an outside left, playing for local teams including Mexborough and Deame Valley Old Boys.

[14] The then City goalkeeper Frank Swift claimed that 'before helping to tuck the blankets over me (on the stretcher) Brookie had pulled my jersey off-about two sizes too big for him- and was ready to keep goal'.

[24][25] Brook and Tilson joined a strong forward line at the club that included three England internationals in Tommy Johnson, Billy Austin and Frank Roberts.

The team also included the England international centre half Sam Cowan and the Scotland captain Jimmy McMullan.

In his first season for Manchester City, Brook played 12 times and scored two goals, helping the team to earn promotion to the First Division.

[36] In the 1930–31 football season City bought the prolific Scottish centre forward Dave Halliday from Arsenal as a replacement for Tommy Johnson.

[5][41] In the 1931–32 season the City team, which now included the Scottish centre forward Alec Herd, managed to reach the semi-final of the FA Cup but were defeated by Arsenal by 1–0 with a goal from Brook's England teammate Cliff Bastin.

In the 1933 FA Cup Final he was part of the Manchester City team that was defeated three goals to nil by Everton, who were captained by his England teammate Dixie Dean.

[55] In the 1934 FA Cup Final Brook set up the winning goal, which was scored by his friend Fred Tilson, to earn City a 2–1 victory over Portsmouth.

[62] Brook had made 'a speculative lob' from the wing, which seemed to change direction in mid-flight, which curled past Stoke goalkeeper Roy John.

[64] The FA Cup winning City team included goalkeeper Frank Swift and left half Jackie Bray, who would both emulate Brook by going on to appear for England.

Swift fainted from nervous exhaustion just before the City team were about to ascend the steps at Wembley to collect the trophy and their winners medals.

[65][66] In the 1934–35 football season Brook scored 17 goals and City finished fourth in the league, ten points behind champions Arsenal.

[67] Billy Meredith stated that 'never has a goal at Maine-road been greeted with more enthusiasm than that which marked Eric Brook's equalising point ten minutes from the finish or a vigorous 1-1 game with the Arsenal'.

[91] In a 1–0 defeat to Sheffield United that season, one journalist praised Brook's enthusiasm stating that he was 'half-back, outside right, outside left and centre-forward just about rolled into one'.

[92] In another game that season, a 2–1 victory against Southampton, Brook scored City's equaliser via a penalty and was described as the 'Peter Pan of outside lefts', who despite being a veteran 'appeared to be forever playing the ball'.

[102] Only five players have appeared for Manchester City more times than Eric Brook: Alan Oakes, Joe Corrigan, Mike Doyle, Bert Trautmann and Colin Bell.

[120] Brook scored the first goal in a 3–0 victory against Ireland which was 'smashed home with a terrific volley from point-blank range, from a Sammy Crooks pass'.

[139] Matthews stated that the behaviour of the Italians affected him, but that 'fortunately we had two real hard nuts in the England side that day in Eric Brook and Wilf Copping who started to dish out as good as they got and more'.

[141] Brook is only one of four England players to have scored more than one goal in a game against Italy, the others being Mick Channon,[142] Gerry Hitchens[143] and Tom Finney.

[101] The record was surpassed in 2010 when six Manchester City players (Joe Hart, Joleon Lescott, Gareth Barry, James Milner, Shaun Wright-Phillips and Adam Johnson) appeared in a 3–1 victory against Switzerland.

[127] In the 1936 British Home Championship, Brook, Ralph Birkett and Tilson each scored in a 3–1 victory over Ireland at Windsor Park.

[149][150] In the game against Scotland, Brook was part of an England forward line which included Sammy Crooks, Bobby Barclay, George Camsell and Cliff Bastin.

[157] In the 1938 British Home Championship Brook played alongside City teammate Sam Barkas in a 5–1 victory over Ireland.

[159] Brook made his final appearance for England in a 2–1 victory over Wales in which his perfect pass set up Willie Hall to score the winning goal.

[178] In the match against Wales, Brook played alongside his Manchester City teammates Frank Swift and Bert Sproston.

[182] As a consequence of the fractured skull that Brook sustained in a car accident while travelling to a wartime international game, he was unable to head a ball and decided to retire from football.

[183][184][185] His England teammates Frank Swift, Raich Carter, Stanley Matthews, Cliff Bastin and Tommy Lawton were able to continue their careers after the war.

[189] Brook is regarded as one of the finest players to have graced the English game and has been inducted into the Manchester City Hall of Fame.

[193] Brook appears in The EFG Bumper Book of QI Annuals in which he is portrayed (imaginarily) with one arm in a sling and another arm in the air, with his hand grasping the Jules Rimet Trophy, with two teammates holding him aloft, in a similar fashion to how Bobby Moore was held aloft by his teammates after England's victory in the 1966 FIFA World Cup final, due to his brace in the 3–2 victory over the then World Champions Italy at the Battle of Highbury in 1934.