Born in Little Berkhamsted, Hertfordshire, he was educated at Eton and New College, Oxford. On 27 August 1922 his father drowned at Bude, Cornwall at the age of 44. A grandfather was governor of the Bank of England between 1908 and 1913. The World War II airborne division commander Frederick 'Boy' Browning was his first cousin.

Johnston obtained a third-class degree in History in 1934 and he then joined the family's coffee business, where he worked until the outbreak of the war. In 1936 he was posted to Brazil but admitted years later that he had little liking or enjoyment of the work. He wanted to be an actor originally. When war was declared in 1939 Johnston joined the 2nd Battalion Grenadier Guards, where he served as a Technical Adjutant and was awarded the Military Cross in 1945. He took part in the Normandy invasion after D-day, with the Guards Armoured Division.

After he was de-mobilised, in November 1945, Brian Johnston joined the BBC in January 1946. He began his cricket commentating career at Lord's for BBC Television in June 1946 at the England v India Test match.

On 22 April 1948 Johnston married Pauline Tozer, formerly of Sheffield. They had five children. The last of his children to be born, a daughter, Joanna, has Down's Syndrome. In these early years, Johnston was an occasional presenter of other BBC shows, including Come Dancing and All Your Own.

Between 1948 and 1952 Johnston presented a live broadcast segment Let's Go Somewhere as part of the Saturday night radio series In Town Tonight. As part of these he stayed alone in the Chamber of Horrors, rode a circus horse, lay under a passing train, was hauled out of the sea by a helicopter and was attacked by a police dog.

He became a regular member of the TV commentary team and, in addition, became BBC cricket correspondent in 1963. From 1965 onwards Johnston split his commentary duties between television (three Tests) and radio (two Tests) each summer. In 1970 Johnston was dropped from the TV commentary team but continued to appear as a member of the team for the radio broadcasts, Test Match Special (TMS). He retired from the BBC in 1972 on his sixtieth birthday, and became a freelance commentator and it was in that capacity that he continued to appear on TMS for the next twenty-two years.

From 1972 to 1987, Brian Johnston presented Down Your Way on BBC Radio Four, in which he visited a different City, Town or Village, interviewing local figures (not necessarily celebrities) and playing a piece of music selected by them at the end of each 'voxpop' interview.

Johnston was responsible for a number of the TMS traditions, including the creation, often using the so-called Oxford "-er", of the nicknames of fellow commentators (for example, Jonathan Agnew is still known as "Aggers", Henry Blofeld as "Blowers" and the late, lamented Bill Frindall as "the Bearded Wonder" ("Bearders"). He once complained on air that he had missed his cake at tea during one match - the TMS team are still sent cakes by listeners.

An incident illustrating Brian Johnston's fast thinking and terrific wit ocurred in about 1951-2 when he was on "In Town Tonight" the BBC programme which included interviews with celebrities who were in London at various times. Brian was interviewing an obnoxious American who, when asked about his visit, made the statement; "London is the asshole of the world". To which Johnston instantly replied "Oh, so you're just passing through, then."

[This obviously was never used on air but I heard the story the next day from the father of a schoolfriend. He was a producer on the show and came home still laughing about it when he arrived and told us. I have never heard any reference to this in any of the various memoirs about him. If any of my schoolfriends, who heard this at the same time as I did, are still alive thry will verify this.(Terry Hallard, Worthing)]

In another famous incident during a Test match at the Oval, Jonathan Agnew suggested that Ian Botham was out hit wicket because he had failed to "get his leg over" (a British slang term meaning to have sex). Johnston carried on commentating (and giggling) for 30 seconds before dissolving into helpless laughter. Among his other gaffes was: when Neil Harvey was representing Australia at the Headingley Test in 1961.

The oft cited quote:

occurred when Michael Holding of the West Indies was bowling to Peter Willey of England in a Test match at The Oval in 1976. Johnston claimed not to have noticed saying anything odd during the match, and that he was only alerted to his gaffe by a letter from "a lady" named "Miss Mainpiece". According to Christopher Martin-Jenkins, the cricinfo biography, Cricinfo - Players and Officials - Brian Johnston and the biography by Johnston's son Barry, Johnston never actually made the remark. His son says "It was too good a pun to resist...but Brian never actually said that he had spoken the words on air." However, this is contradicted by an account offered by Henry Blofeld, who claims to have been present at the time. It is perhaps worth noting though that, with Blofeld's recollection of the score being 81-7 when the remark was made, England had a healthy first innings, and in the second Willey was the fourth wicket. In the second innings Peter Willey faced 11 balls and was caught by Gordon Greenidge off the bowling of Vanburn Holder. The two batsman whose wickets fell either side of Willeys were both bowled by Michael Holding so it is reasonable to assume that Willey did face some balls from Holding. The score was 4-77 when Willeys wicket fell. A popular cricket website, Holdingwilley.com, has named itself after this well-known cricket anecdote, although the site is a general cricket website and doesn't focus on that incident alone.

Johnston variously presented and participated in a wide range of BBC radio and television programmes. These included radio programmes such as In Town Tonight, Down Your Way, Trivia Test Match, and the Royal Command Performance of The Good Life in 1978. He also commentated on events like the funeral of King George VI, the coronation of Elizabeth II and the wedding of HRH The Prince of Wales and Lady Diana Spencer in 1981. Johnston was also for several years one of the presenters of the Channel 4 magazine programme for the over sixties Years Ahead" along with Robert Dougall, Zena Skinner and Paul Lewis.

He appeared as himself in the 1952 British film Derby Day.

Johnston was a great fan of the British Music Hall and revelled in its often mildly risqué 'schoolboy humour'. An Evening with Johnners, a one-man show that he performed towards the end of his life, included many excruciating jokes, as well as his broadcasting and cricket reminisces. A recording of one of these shows was released and reached #46 on the UK Albums Chart in March 1994.

He was appointed OBE in 1983 and CBE in 1991.

Johnston's informal and humorous style was very popular. When he died on 5 January 1994, a month after suffering a massive heart attack, The Daily Telegraph described him as "the greatest natural broadcaster of them all" and John Major, the British Prime Minister and cricket fan, said that "Summers simply won't be the same without him". Brian Johnston’s memorial service was held at a packed Westminster Abbey on 16 May 1994. Over 2,000 people were present. The following year the Brian Johnston Memorial Trust was established to promote cricket in schools and youth clubs, to help young cricketers in need of financial support, and to further disabled cricket. The trust is now part of the Lord's Taverners.