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.Layer Road's first League game to finish under lights was on August 24th 1959 when 9,689 watched the 2-2 draw with Grimsby.
The main bonus for the season was that Martyn King was on the verge of completing his National Service and was available for every game.
King responded in fine style by equalling McCurley's 30 League goals in-a-season club record including a trio of hat tricks.
United lost just two games at Layer Road but won just three on their travels and finished 1959/60 a creditable 9th in the table.
The 1960/1 season, however, proved disastrous.
Average attendances plummeted from 7,810 to 4,954 as United lost ten home games finishing in 23rd position and suffering relegation to the Fourth Division.
Obtaining just one point from eleven games, including seven straight defeats, the U's hit rock bottom in October 1960 and they never managed to climb out of the bottom four.
Remarkably King still managed to notch 25 League goals including a hat-trick against Chesterfield in the final game of the season that attracted a new all-time low attendance of just 3,141.
United also conceded 101 League goals - the only time that this landmark has been suffered.
Colchester did enjoy some early season success when in the inaugural League Cup competition they comprehensively defeated First Division Newcastle 4-1 at Layer Road in front of 9,130 before bowing out to Southampton in Round Two.
But, at the end of the season, Fenton wielded his relegation axe and the club were, alarmingly, over £3,300 in the red. Out went ten players including Langman, Milligan and Tommy Williams.
United commenced their 1961/2 campaign by going unbeaten in their first nine League games and scored 31 goals in the first eight home games to top the Fourth Division.
Tragedy struck in October 1961.
Whilst The U's were playing at York the young son of full-back Tommy Millar drowned in a garden pond accident. Colchester failed to win any of their next five games and slipped to third in the table.
After a Boxing Day 4-1 defeat at Bradford City, United set their club record victory in the return fixture with The Bantams on December 30th 1961.
Both King and his strike partner Bobby Hunt scored four goals each, and Bobby Hill one, as The U's ran out 9-1 winners.
A 4-0 win at Accrington Stanley saw United regain top spot from Wrexham, but within weeks Accrington folded and United's 3-2 and 4-0 wins were wiped from the records.
Losing at Millwall and drawing at Wrexham cost United the championship. Millwall took the title by one point from runners-up Colchester with 11 defeats on the road costing the U's dearly.
Amongst U's record 104 League goals scored, 78 of them at Layer Road, King broke his own seasonal record with 31 only to be outdone by partner Bobby Hunt who bagged a new record 38 League goals including three hat-tricks - two of which were four goal hauls.
Stability was the key with just 17 players used and eight of those played over 40 of the 44 games possible.
Support was slightly up with an average of 5,341 although the 50 year local disparity reached one of its peaks when Ipswich won the First Division championship.
Despite still being £2,000 in the red, United were not about to sell their prize asset Bobby Hunt when Newcastle came in with a £17,000 offer (about £580,000 today based on the average earnings index).
Colchester made their debut in the new Anglia TV football programme Match of the Week when highlights were shown of the October 13th 1962 Layer Road defeat to Crystal Palace.
Once again, King led the League scoring charts with 26 goals while Bobby Hunt scored 19. A leaky defence, U's conceded 93 goals, meant that mid-table was the best U's could hope for.
They were also unceremoniously dumped out of the FA Cup by Isthmian League Wimbledon.
The next season proved to be one of change. Out went manager Benny Fenton who took over the manager's role at Orient in November 1963.
Replacing him was former Stoke and England centre-half Neil Franklin.
Franklin had been a regular alongside Billy Wright in the England side just after the War, but blotted his CV when he embarked on a fools gold trip to Colombia to become part of an underworld-funded attempt to attract the World's best players to play in a renegade League.
The competition was not FIFA sanctioned, the financial promises not met and Franklin returned to the UK to face a lengthy FA ban.
His first transfer at Layer Road was to sell Bobby Hunt to First Division-bound Northampton for £20,000 (around £650,000 based on the average earnings index).
Hunt already had 20 goals from 33 League games when he left with King reaching 18 by the end of a disappointing 16th placed campaign. United had claimed another First Division scalp when beating Fulham 5-3 in the League Cup at Layer Road but crashed out to Workington at the Third Round stage.
The biggest surprise came when Peter Wright was not on the retained list.
Playing his entire career as a part-timer Wright set the record for appearances in a United shirt completing 453 League and Cup games scoring 99 goals. He was only 30 at the time of his release.
Franklin also sold King to Wrexham in October 1964. This, and the Hunt sale, did not impress the U's faithful.
Bringing in 14 new players in just a season and a half proved too much of an upheaval for United.
The loss of their prolific strike force was naturally the most devastating blow and only 50 League goals were scored. Inevitably United struggled throughout the season.
Franklin's first signings Derek Trevis and Duncan Forbes were ever-presents with Billy Stark being leading scorer with just 13 League goals.
Colchester were relegated back to the Fourth Division with Franklin having already being given a year's contract extension mid-season.
Average attendances hit an all-time low of 3,655 and the Supporters Club could only muster 997 members - a far cry from the heady days of the late 1940s.
As they did four years previously, United bounced back up from the Fourth Division at the first attempt although it was not until the final day of the season that they sealed promotion.
Franklin brought in Reg Stratton to lead his attack and the forward responded with 17 League goals. United won ten games on their travels, a new club record, and lost just three times at Layer Road.
Colchester led the table at Easter 1966 despite being held twice by rivals Luton with the Layer Road holiday fixture attracting 10,200.
Subsequent defeats to promotion contenders Darlington (twice) and Torquay saw United drop to fourth place prior to the last game of the season.
A disastrous 2-1 defeat at mid-table Newport had U's fans biting their nails as Luton were only a point behind and their game at Chester had kicked off 15 minutes later. In the end the game finished 1-1 and with the U's, Tranmere and the Hatters tied on 56 points it was down to goal average to separate the sides.
Franklin's side pipped Tranmere by 0.08 (equivalent to about 6 goals difference in today's rules).
The season was also notable as player replacements were allowed for the first time.
Ray Price became United's first substitute when he took over from Ted Philips after 85 minutes of the September 18th 1965 home fixture with Rochdale. Gates had improved, with on-the-pitch success, to an average of 5,148.
Franklin boosted his squad with the signings of forwards Peter Bullock and Ken Hodgson. The moves proved profitable as the pair scored 15 and 16 League goals respectively.
Fellow striker Stratton helped himself to 24 goals and it was something of a surprise that U's only finished mid-table.
Franklin suggested that the 1966/7 season would be one of consolidation in readiness for a push for the elusive Second Division place that Colchester desired.
In a fantastic season for FA Cup football, Colchester were dreadful in the League. A difficult trip to Torquay earned United a First Round replay at Layer Road which they won 2-1 to set up a mouth-watering local derby at Chelmsford.
New Writtle Street was packed with 16,400 as United despatched the Southern Leaguers by 2-0.
Once again Layer Road hosted a top flight side as West Bromwich Albion visited in the Third Round. An all ticket crowd of just under 16,000 saw United take an early lead through Stratton only for the Baggies to equalise with a questionable penalty.
Both Stratton and John Mansfield, in the last minute, had the ball in the Albion net but both were dubiously ruled out. United sank by 4-0 at The Hawthorns in the replay watched by 40,008.
With all the attention on the FA Cup, U's League form had dipped. From being within a striking distance of a promotion place, Colchester lost 15 of their remaining 22 games after Boxing Day 1967 winning just once.
Crowds plummeted to an average of 3,993 with a new all-time low of 2,483 watching the final day 5-1 Layer Road annihilation by Peterborough.
Colchester's third relegation in eight seasons was too much and Franklin was sacked just two days after the curtain fell on the forgettable campaign.
Colchester's new manager was Dick Graham. He had led Crystal Palace from the Fourth to the Second Division and his mandate was clear. Graham needed to emulate his work at Selhurst Park.
After seven games and one point Graham savaged his inherited squad, axing six players and selling Duncan Forbes and Derek Trevis for a combined fee of £19,000.
He brought in a number of players including goalkeeper Tony Macedo and former Spurs double-winner Terry Dyson. The U's proceeded to earn 33 points from a possible 42 reaching fourth place.
A disappointing Easter period when they faced rivals Bradford, Halifax and Swansea realised just two draws and United finished 1968/9 in 6th position just four points short of promotion.
Graham then adopted a policy of employing an older more experienced player. He declared: "I believe in signing players who have done something big and giving them a new lease of life."
He chose Bobby Cram, formerly of West Brom, and hitherto playing in Canada, to become his captain for his second season at the helm and paid £5,000 for forward Ken Jones to replace the unfortunate injury-hit Roy Massey.
An eleven game unbeaten home run gave United hope of a promotion push but a crippling injury list, even trainer Dennis Mochan had to dig out his boots, was a bridge too far.
United finished tenth but no-one could have imagined the world fame Graham and his ageing side would acquire as the 1960s ended and the new decade began.