Instead, Bosley became a mainstay on the small screen. He began in the medium in 1955 as the Knave of Hearts in a NBC "Hallmark Hall of Fame" production of "Alice in Wonderland" and was memorable as Teddy Brewster, who thinks he is Teddy Roosevelt, in the 1962 Hallmark/NBC TV version of "Arsenic and Old Lace". Bosley has made dozens of episodic guest-starring appearances through the years, as well as appearing as a regular on more than 10 series, beginning with "That Was the Week That Was" (1964), a topical revue show. He supported Debbie Reynolds in her NBC series effort in 1969, was a Dean Martin regular during the 1971 season, Sandy Duncan's boss on her short-lived series in 1972, and provided the voice of the father in the syndicated animated sitcom "Wait 'Til Your Father Gets Home" (1972-74). His signature role of Howard Cunningham, the unabashed Ike-liking father of Richie (Ron Howard) who eventually learned to love The Fonz (Henry Winkler) as a surrogate son as well, came in 1974. Howard's bite was never as tough as his grumble and he was among the last of the touchstone American suburban dads on TV. Following the 1984 demise of "Happy Days", Bosley joined the cast of "Murder, She Wrote" (CBS 1984-88) in the recurring role of Amos Tucker, the downeast-accented sheriff who was never quite as smart as Angela Lansbury's Jessica Fletcher when it came to solving the frequent murders in Cabot Cove. Bosley subsequently played Father Frank Dowling, a crime-solving priest, first in an NBC TV-movie/pilot and then in the series, "The Father Dowling Mysteries" (NBC, 1989; ABC 1990-91).

Bosley has also appeared in numerous TV-movies and dramas, beginning with "A Step Out of Line" (CBS, 1971). He was memorable as the sweatshop manager who loves his little daughter in "The Triangle Factory Fire Scandal" (NBC, 1979), and he played Ben Franklin in the syndicated miniseries "The Bastard" (1978) and its 1979 sequel, "The Rebels." He has appeared in more than one dozen feature films, albeit with less lasting power than his TV work. Bosley's first role of note was in "Love With the Proper Stranger" (1963), as the pudgy restaurant owner who wants to marry Natalie Wood. He was the bickering, incarcerated General Pennypacker in "The Secret War of Harry Frigg" (1968) and the police lieutenant investigating the disappearance of a family in Bette Davis' unfortunate last film, "Wicked Stepmother" (1989). Bosley has also appeared in numerous TV commercials, and does voice-overs for many others, including Hanna-Barbera's "Yogi's Gang" (1973).