St. Johns County Homes With Guest House

Interested in the extra living space homes with a guest house provide? Featured here are all St. Johns County homes for sale with a guest house. If you’re interested in any of the St. John's County guest house home listings that you see below, just click the "Ask a Question" button when viewing the details of that property. Our St. John's County real estate agents can provide you with disclosures, past sales history, dates and prices of properties recently sold nearby, and other details related to St. John's County homes with a guest house.

And if you'd like to stay up-to-date on St. John's County homes with a guest house, we also invite you to register for a free account so that you can receive email alerts whenever new listings hit the market that fit your search criteria, allowing you to stay one-step ahead of other buyers in the area. And remember to call or text us directly with any additional questions you have about buying or selling a home in St. John's County, Florida. 

Search St. Johns County Homes With Guest House

• All Listings
• $100,000 - $200,000
• $200,000 - $300,000
• $300,000 - $400,000
• $400,000 - $500,000
• $500,000 - $600,000
• $600,000 - $700,000
• $700,000 - $800,000
• $800,000 - $900,000
• $900,000 - $1,000,000
• Over $1,000,000

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Newest First

New

$449,000

150 Seagate Lane S, St. Augustine

0 Beds 0 Baths 0 SqFt Land MLS® # 2163999

New

$1,290,000

167 Herons Nest Lane, St. Augustine

4 Beds 3 Baths 2,833 SqFt Residential MLS® # 2163989

New Pending

$375,000

1578 Stillwater Boulevard, St. Johns

3 Beds 2 Baths 1,886 SqFt Residential MLS® # 2133537

New Open House

$899,000

817 Eagle Point Drive, St. Augustine

5 Beds 4 Baths 3,246 SqFt Residential MLS® # 2163986

New

$385,000

7750 A1a S 151, St. Augustine Beach

1 Bed 1 Bath 950 SqFt Residential MLS® # 2163984

New

$579,900

311 Rum Runner Way, St. Johns

4 Beds 3 Baths 2,558 SqFt Residential MLS® # 2163980

New

$209,000

860 S Black Cherry Drive, St. Johns

3 Beds 3 Baths 1,468 SqFt Residential MLS® # 2149187

New

$350,000

104 Logrono Court, St. Augustine

4 Beds 2 Baths 1,919 SqFt Residential MLS® # 2163977

New

$829,000

106 Lucerne Court, St. Augustine

5 Beds 4 Baths 3,280 SqFt Residential MLS® # 2163972

New

$1,449,000

397 Lakeview Pass Way, St. Johns

6 Beds 5 Baths 4,502 SqFt Residential MLS® # 2157809

$2,949,049

48 A Roscoe Boulevard N, Ponte Vedra Beach

4 Beds 3 Baths 3,243 SqFt Residential MLS® # 2161571

New

$1,300,000

8000 County Road 13 N, St. Augustine

0 Beds 0 Baths 0 SqFt Commercial Sale MLS® # 2163932

New

$939,583

103 Junction Avenue, St. Johns

4 Beds 4 Baths 31,966 SqFt Residential MLS® # 2163928

New Pending

$1,387,000

144 Clearlake Drive, Ponte Vedra Beach

5 Beds 4 Baths 3,592 SqFt Residential MLS® # 2134087

New

$675,000

629 Melrose Abbey Lane, Fruit Cove

6 Beds 4 Baths 3,544 SqFt Residential MLS® # 2163917

New Open House

$599,000

124 Beachside Drive, Ponte Vedra

3 Beds 2 Baths 1,598 SqFt Residential

Open House

Fri, Sep 11th, 2026 @ 1pm - 3pm

MLS® # 2163918

New

$508,990

272 Hasler Avenue, St. Augustine

4 Beds 4 Baths 2,028 SqFt Residential MLS® # 2163911

New

$556,990

66 Stiffs Mill Lane, St. Augustine

4 Beds 3 Baths 2,521 SqFt Residential MLS® # 2163908

New Open House

$548,900

109 Bay Hill Court, Ponte Vedra Beach

2 Beds 2 Baths 1,578 SqFt Residential

Open House

Sat, Sep 12th, 2026 @ 11am - 1pm

MLS® # 2163909

New

$439,990

209 Superior Boulevard, St. Augustine

3 Beds 3 Baths 1,714 SqFt Residential MLS® # 2163904

New

$439,990

143 Superior Boulevard, St. Augustine

3 Beds 3 Baths 1,714 SqFt Residential MLS® # 2163901

New Pending

$675,830

907 Caiden Drive, Ponte Vedra

3 Beds 3 Baths 2,340 SqFt Residential MLS® # 2163899

New

$1,850,000

103 Relajado Way 3, St. Augustine

3 Beds 5 Baths 2,752 SqFt Residential MLS® # 2163898

New

$700,000

10017 Sawgrass Drive E, Ponte Vedra Beach

2 Beds 2 Baths 1,424 SqFt Residential MLS® # 2163892

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