The elevation to the Football League meant that, as predicted by Ted Davis in 1937, The U's would have to release or pay for the players that were registered with other League clubs.
Allen signed Reg Stewart and Bill Layton and a further £8,000 was spent on recruiting ten new players.
Colchester's first-ever League game was against old Southern League foes Gillingham at Priestfield on August 19th 1950. A crowd of 19,542 witnessed a 0-0 draw.
Five days later Bob Curry scored United's first-ever League goal in a 1-1 draw at Swindon.
However, it was not until August 31st that Layer Road enjoyed its first U's goal. Arthur Turner struck five minutes into a 4-1 win in the return game with Swindon.
In fact, Colchester remained unbeaten in their first seven games. This run equalled a record for new clubs entering the Football League set by Aberdare Athletic in 1921/2.
The U's occupied second spot in the table before the bubble burst with nine defeats in the next 10 games. Colchester finished the 1950/1 season in a creditable 16th position and averaged 10,573 through the Layer Road turnstiles.
It would be the only time that Layer Road hosted a five-figure average.
Prolific marksman Keeble had the distinction of becoming Layer Road's first hat trick hero when he grabbed all the goals in a 3-0 win over Plymouth on March 17th 1951.
The 1951/2 season started dreadfully with six defeats in the opening seven games due mainly to an injury-ravaged squad.
United sat rooted to the foot of the Third Division South table, but a mid season revival including completing the double over local rivals Ipswich hoisted United to 10th in the final standings.
Keeble became United's first big time transfer when he moved to First Division Newcastle for a massive £15,000 fee. Based on average earnings, that figure today would be just over £1m.
Colchester reached the FA Cup Third Round but were beaten at Second Division Barnsley.
Having lost Curry and Turner through retirement, and then Keeble, it was inevitable that Colchester's attack needed new blood. Allen signed Kevin McCurley for £750 from Liverpool and Johnny Church from Norwich.
The U's averaged just shy of 9,500 for home games and at the conclusion of the campaign, Colchester embarked on an undefeated three-match tour of Holland.
A suggestion was raised that Layer Road should be provided with floodlights but at a cost of £500 the notion was put on hold
The 1952/3 season kicked off with a 14,674 Layer Road crowd witnessing a 0-0 draw with Ipswich and United hovered around mid table for the first half of the season and once again reached the Third Round of the FA Cup.
Disposing of non-Leaguers Weymouth and Llanelli, it was a Yorkshire club again that ended Colchester's run. Securing a 2-2 draw at Second Division Rotherham, U's lost the replay 2-0 at Layer Road missing out on a potential tie with Newcastle.
A disastrous run of just one point from the last six games then saw United slip from 13th to just one place and two points above the re-election zone.
McCurley had justified Allen's outlay with 19 goals and the season was significant with the introduction of a young winger by the name of Peter Wright.
The need for floodlights was emphasized when just 3,382 watched the re-arranged Thursday March 19th 1953 afternoon fixture with Crystal Palace.
Criticised by supporters for his style of play and unwilling to implement the Board's call for a reduction in playing staff, Allen resigned on May 2nd 1953.
The Board shortlisted three names for the vacant managerial position and, in line with their cost reduction policy, appointed Ron Meades as player-manager.
Meades had presented his CV claiming to have been with Cardiff and more recently manager of Western League side Wadebridge Town.
A piece of investigative journalism by U's reporter Arthur Wood revealed that Meades was a fraud and after four days in charge Meades was asked to leave by a very embarrassed United hierarchy.
Jack Butler, a former Arsenal player, was hurriedly appointed manager. Butler had been coaching in Belgium with the Royal Daring Club and had been in charge of the Belgian national team between 1935-40 leading them to the 1938 World Cup Finals.
Butler had little time to prepare his side and a 13-game run without winning saw United in 23rd spot.
Crowds plummeted to 7,762 and the club had to go cap in hand to the Football League to apply for re-election after finishing 10 points adrift of the safety of 22nd place.
Fortunately The U's were still endeared to their fellow League clubs and they polled 45 votes. Walsall, wooden-spoonists, took 32 votes easily seeing off the best non-League application of Peterborough who attracted 18 votes.
From being prolific scorers in their early history United scored just 50 League goals in 1953/4.
Butler's squad for the new season numbered 28, 16 of whom were full-time professionals and the remainder involved in National Service or were part-timers.
The Supporters Club had dwindled to just 5,065 members and attendances continued to plummet.
Another dreadful run of eight consecutive defeats saw United locked at the bottom of the League on Christmas Day 1954.However, a four-game turn about in form saw United rise out of the re-election places, but the U's plight was having a drastic effect on Butler's health.
After falling ill in November he was given indefinite leave until the end of his contract in 1956.
Suffering from a nervous breakdown Butler resigned in January 1955 with club secretary Claude Orrin heading a selection committee whilst a new manager was sought.
Despite United's poor recent form they were a sought-after proposition attracting 48 applications. The Board chose Benny Fenton to be player/manager, but the damage for the season was already done.
The initial boost of Fenton's appointment tailed off and United picked up just one point from their last eight games.
Once again Colchester had to go to the Football League to retain their status, accompanied by Walsall for the second successive season.
Both were successful and the manager announced that The U's needed a massive clear out.
Fenton assembled his own squad for 1955/6. He began with Percy Ames who would have an incredible run of appearances in United's goal and then Fenton gained a reputation for spotting players in Scottish Junior football with the acquisition of John Fowler, Sammy McLeod and Bobby Hill.
After an initial bedding-in period, Fenton turned his team into an exciting attacking side. U's scored 76 times with McCurley (30 goals) and strike partner Ken Plant (16 goals) both grabbing two hat tricks apiece.
Safe from the ignominy of re-election, Fenton spent the period covering the last seven games scouting for new players.
United finished 12th, their best-ever League finish, and hopes were high that Colchester could emulate Ipswich and climb into the Second Division, albeit that Town only lasted one season at the higher level.
The club also played their first-ever League game under floodlights when they beat Reading 3-1 at Elm Park on February 28th 1955.
Layer Road was still bereft of floodlighting although lights had been installed for training purposes.
1956/7 proved to be Colchester's best finish in their history, a position that was not bettered until 2006. For most of the season United were certainties for promotion.
They played with flair and went 20 League games undefeated between December 1956 and Easter 1957.
During this spell United hosted third-placed rivals Ipswich at Layer Road. Colchester had a seven point advantage, although Town had a game in hand. A record crowd for a Layer Road League game - 18,559 - witnessed a 0-0 draw.
Over 4,000 were turned away and 120 fans watched from the Popular Side roof (Barside as is now).The game went down in United folklore when Fenton missed a 21st minute penalty.
The notion survived well into the next century that Fenton deliberately missed the penalty because United could not afford to compete at Second Division level.
In fact, Town keeper Roy Bailey magnificently turned the spot kick around the post. A 2-1 win over second-placed Torquay, who trailed by four points as a result, put United in pole position in front of yet another bumper Layer Road crowd of 12,555.
But then the loss of Bob Dale and Chic Milligan dented United's run-in. Three consecutive draws allowed Torquay to close the gap to one point with Ipswich five points adrift.
Then disaster struck. Over Easter 1957, United lost three away games at Millwall, Walsall and Swindon.
Colchester won their final game of the season 2-0 against Watford to go top, but both Ipswich and Torquay's final games were 24 hours later. Both won, United slipped to third and Ipswich went up as champions level with Torquay and a point ahead of The U's.
The next 50 years of professional football either side of the Essex/Suffolk border was determined from that point on.
With Football League re-organisation on the agenda U's first priority for 1957/8 was to finish in the top twelve as those clubs would join the top twelve in the Third Division North to form the new country-wide Third Division. The remainder would form the Fourth Division.
Fenton's squad suffered from call ups to National Service and he recruited forwards Neil Langman from Plymouth for £6,500 and John Evans from Liverpool for £4,000 in November 1957.
Birmingham offered £10,000 for United's exciting Peter Wright but the player chose to remain part-time.
It was not until the last game of the season that a 4-2 Layer Road win over Southampton secured 12th place and that coveted place in the Third Division.
A very good fifth placed finish in 1958/9, nine points behind second-placed Hull, included a club record 8-2 win over Stockport on October 4th 1958.
The highlight of the season, however, was another FA Cup run. Early round victories over Bath, Yeovil and Chesterfield brought the mighty Arsenal to Layer Road in the Fourth Round. The replay win at Yeovil by 7-1 remains a club record away win.
For the first time the Police set a limit on crowd numbers at Layer Road - 16,000 witnessed a 2-2 draw and in the return 62,686 saw The Gunners run out 4-0 winners on a frost-bound pitch obscured by thick fog.
Langman and Evans repaid their transfer fees with 27 and 16 goals respectively.
What's more, the proceeds from the Arsenal ties paved the way for floodlights to be installed at Layer Road.
