St. John's County Homes With Guest Suite

Are you a home buyer who could use the extra living space a guest suite provides? Featured here are all St. John's County homes for sale with a guest suite. If you’re interested in any of the St. John's County guest suite 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 suite.

And if you'd like to stay up-to-date on St. John's County homes with a guest suite, 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. John's County Homes With Guest Suite

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New
114 Eagles Landing Lane, St Augustine

$439,700

114 Eagles Landing Lane, St Augustine

3 Beds 2 Baths 1,591 SqFt Residential MLS® # 2027827
New Pending
50 Carbonell Place, St Augustine

$385,000

50 Carbonell Place, St Augustine

3 Beds 2 Baths 1,864 SqFt Residential MLS® # 2027811
New
1329 Wekiva Way, St Augustine

$430,000

1329 Wekiva Way, St Augustine

4 Beds 2 Baths 1,768 SqFt Residential MLS® # 2027808
New
1130 Salt Creek Drive, Ponte Vedra Beach

$1,150,000

1130 Salt Creek Drive, Ponte Vedra Beach

3 Beds 3 Baths 2,452 SqFt Residential MLS® # 2027784
New
119 Spinner Drive, Ponte Vedra

$675,000

119 Spinner Drive, Ponte Vedra

3 Beds 3 Baths 2,124 SqFt Residential MLS® # 2027767
New
2435 Ponte Vedra Boulevard, Ponte Vedra Beach

$4,122,000

2435 Ponte Vedra Boulevard, Ponte Vedra Beach

5 Beds 5 Baths 3,923 SqFt Residential MLS® # 2027765
New
135 Herons Nest Lane, St Augustine

$899,000

135 Herons Nest Lane, St Augustine

4 Beds 3 Baths 2,717 SqFt Residential MLS® # 2027750
New
352 W Adelaide Drive, Fruit Cove

$499,900

352 W Adelaide Drive, Fruit Cove

4 Beds 4 Baths 2,601 SqFt Residential MLS® # 2027739
New
232 Atlas Drive, St Augustine

$625,000

232 Atlas Drive, St Augustine

4 Beds 3 Baths 2,481 SqFt Residential MLS® # 2027733
New
326 Willow Winds Parkway, St Johns

$612,000

326 Willow Winds Parkway, St Johns

4 Beds 3 Baths 2,543 SqFt Residential MLS® # 2027731
New
220 Dark Horse Lane, Hastings

$1,845,000

220 Dark Horse Lane, Hastings

5 Beds 3 Baths 3,415 SqFt Residential MLS® # 2027727
New
490 Timber Lgt Trail, Ponte Vedra

$659,999

490 Timber Lgt Trail, Ponte Vedra

2 Beds 2 Baths 1,626 SqFt Residential MLS® # 2027721
New
283 Stonewell Drive, St Johns

$975,000

283 Stonewell Drive, St Johns

5 Beds 5 Baths 3,984 SqFt Residential MLS® # 2027709
New
616 Hummingbird Court, St Johns

$385,000

616 Hummingbird Court, St Johns

3 Beds 2 Baths 1,600 SqFt Residential MLS® # 2024343
New
333 Palazzo Circle, St Augustine

$599,900

333 Palazzo Circle, St Augustine

5 Beds 4 Baths 2,830 SqFt Residential MLS® # 2027705
New
224 San Nicolas Way, St Augustine

$585,000

224 San Nicolas Way, St Augustine

3 Beds 2 Baths 1,648 SqFt Residential MLS® # 2027699
New
52 Falcon Ridge Road, St Augustine

$391,900

52 Falcon Ridge Road, St Augustine

3 Beds 2 Baths 1,596 SqFt Residential MLS® # 2027669
New
84 San Telmo Court, St Augustine

$789,000

84 San Telmo Court, St Augustine

5 Beds 4 Baths 3,381 SqFt Residential MLS® # 2027676
New
607 Twentieth Street, St Augustine

$599,000

607 Twentieth Street, St Augustine

2 Beds 2 Baths 968 SqFt Residential MLS® # 2027651
New
136 Crown Wheel Circle, St Johns

$539,500

136 Crown Wheel Circle, St Johns

3 Beds 2 Baths 2,023 SqFt Residential MLS® # 2027626
New
2400 E Hawkcrest Drive, St Johns

$675,000

2400 E Hawkcrest Drive, St Johns

4 Beds 2 Baths 2,585 SqFt Residential MLS® # 2026858
New
141 Greendale Drive, Ponte Vedra

$579,000

141 Greendale Drive, Ponte Vedra

3 Beds 3 Baths 1,893 SqFt Residential MLS® # 2027573
New
1105 Rustic Mill Drive, St Augustine

$390,000

1105 Rustic Mill Drive, St Augustine

2 Beds 2 Baths 1,581 SqFt Residential MLS® # 2025951
New
46 Glenwood Street, Ponte Vedra

$679,900

46 Glenwood Street, Ponte Vedra

4 Beds 3 Baths 2,234 SqFt Residential MLS® # 2025791

St. John's County Homes With Guest Suite Market Data

St. John's County Homes With Guest Suite housing market statistics: As of May 24, 2024 there are currently 3,105 properties for sale in St. John's County Homes With Guest Suite, with an average asking price of $826,848. The highest-priced property is $17,875,000 and the lowest-priced property can be purchased for $137,500. St. John's County Homes With Guest Suite listings have an average price of $316 per square feet, based on listings with 4 beds, 3 baths, and 2,474 square feet of living space.