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    Destin, FL Office Buildings for Sale

    9 results
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    Destin Office Building with Credit
    $1,425,000

    Destin Office Building with Credit

    135 Benning Dr, Destin, FL 32541

    Large, centrally located Destin property with renovation credit.

    • $100,000 seller credit for renovations.
    • Large property offering a customizable interior layout.
    • Centrally located in Destin with high visibility.
    • Located along the planned Legion Drive extension.
    • Two parking lots and three curb cuts.
    Updated: Apr 29, 2025
    View details
    Destin West End Office Space
    $817,500
    4,314 SF

    Destin West End Office Space

    150 Azalea Dr, Destin, FL 32541

    Prime Destin Office: 4,029 SF, For Sale

    • 4,029 square feet of professional office space in Destin, FL.
    • High‑end interior finishes including 12' ceilings and custom design.
    • Seller may leave substantial existing furniture; $817,500 asking price.
    Updated: Feb 5, 2025
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    Destin Office Building: Prime Location
    $3,200,000
    11,340 SF

    Destin Office Building: Prime Location

    Class A, three-story office building; excellent visibility.

    4608 Opa Locka Ln, Destin, FL 32541
    View details
    Destin Commercial Building For Sale
    $2,995,000
    13,396 SF

    Destin Commercial Building For Sale

    Prime Destin location, 9,350 SF office space, ample parking.

    35000 Emerald Coast Pkwy, Destin, FL 32541
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    Single-Story Office Building on Harbor
    $850,000

    Single-Story Office Building on Harbor

    Single-story office building with front and rear parking.

    727 Harbor Blvd, Destin, FL 32541
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    Class A Office Building
    $4,995,000

    Class A Office Building

    Class A office building in Destin's Regatta Commons.

    4458 Legendary Dr, Destin, FL 32541
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    Class A Office Building
    $4,950,000
    22,676 SF

    Class A Office Building

    Premier office building in Destin's Regatta Commons.

    Legendary Dr, Destin, FL 32541
    View details
    Harbor Blvd Commercial Office Buildings
    $1,950,000
    5,258 SF

    Harbor Blvd Commercial Office Buildings

    Two office buildings on 0.46 acres with parking.

    725 Harbor Blvd, Destin, FL 32541
    View details
    Destin Class A Office Building
    $4,224,000

    Destin Class A Office Building

    Fully leased Class A office building in the heart of Destin.

    4635 Gulfstarr Dr, Destin, FL 32541
    View details
    Based on your search, we've compiled 68 Potential Opportunities for your consideration. Besides 9 Active listings in Destin, FL, we suggest exploring several alternatives: 4 properties in Nearby Cities, and similar 54 Off-Market properties to explore as potential leads, plus 1 Land Listings that present a potential for development.

    Explore Opportunities in Nearby Cities

    Here are 4 Similar properties we found in Nearby Locations for your consideration.

    Soundfront Commercial Condominium Opportunity
    $3,000,000
    10,307 SF

    Soundfront Commercial Condominium Opportunity

    Unique commercial property with multi-use building and office building.

    205 Brooks St SE, Fort Walton Beach, FL 32548
    View details
    Class A Office Investment Property
    $1,850,000

    Class A Office Investment Property

    Prime corner location, modern construction, and stable long-term tenants.

    21 Hollywood Blvd, Fort Walton Beach, FL 32548
    View details
    Historic Two-Story Office Building
    $499,900
    4,600 SF

    Historic Two-Story Office Building

    Charming two-story office building in historic downtown Milton.

    5220 Willing St, Milton, FL 32570
    View details
    Downtown Milton Commercial Building For Sale
    $195,000
    1,069 SF

    Downtown Milton Commercial Building For Sale

    Commercial building in downtown Milton, convenient to Hwy 90.

    5234 Willing St, Milton, FL 32570
    View details

    Potential Development Sites for Consideration

    Can't find the perfect fit? These Land listings present an alternative path: the potential to develop a property for your specific goals.

    Important: These AI-suggestions are a starting point, not a guarantee of permitted use. All zoning, permitting, and land use information must be independently verified by you with the appropriate local authorities before making any commitments.

    Destin Land Investment Opportunity
    $1,775,000
    1.40 Acres

    Destin Land Investment Opportunity

    Five contiguous parcels of vacant land in Destin, Florida.

    523 Sea Hills Dr, Destin, FL 32541
    View details

    Explore Off-Market Properties in Destin, FL

    Consider similar Off-Market properties in Destin, FL. You may contact the owners directly to inquire about their potential intentions to sell. To help you make a strong first impression, we can assist by reaching out to these owners with compelling proposals created using our AI tool.

    1012 Airport Rd, Unit STE-1

    1012 Airport Rd, Unit STE-1

    OFFICE BUILDING • 1,250 SF
    Value Estimation
    $525,000
    1012 Airport Rd, Destin, FL 32541-2898
    View details
    151 Regions Way

    151 Regions Way

    OFFICE BUILDING • 7,392 SF
    Value Estimation
    $1,020,000
    151 Regions Way, Destin, FL 32541-5106
    View details
    151 Regions Way

    151 Regions Way

    OFFICE BUILDING • 3,830 SF
    Value Estimation
    $1,005,000
    151 Regions Way, Destin, FL 32541-5106
    View details
    215 Mtn Dr Ste, Unit 102

    215 Mtn Dr Ste, Unit 102

    OFFICE BUILDING • 1,290 SF
    Value Estimation by Request
    215 Mtn Dr Ste, Destin, FL 32541-2346
    View details
    215 Mtn Dr Ste, Unit 101

    215 Mtn Dr Ste, Unit 101

    OFFICE BUILDING • 640 SF
    Value Estimation by Request
    215 Mtn Dr Ste, Destin, FL 32541-2346
    View details
    215 Mtn Dr Ste, Unit 103

    215 Mtn Dr Ste, Unit 103

    OFFICE BUILDING • 1,432 SF
    Value Estimation by Request
    215 Mtn Dr Ste, Destin, FL 32541-2346
    View details
    215 Mtn Dr Ste, Unit 109

    215 Mtn Dr Ste, Unit 109

    OFFICE BUILDING • 1,130 SF
    Value Estimation by Request
    215 Mtn Dr Ste, Destin, FL 32541-2346
    View details
    215 Mtn Dr Ste, Unit 107

    215 Mtn Dr Ste, Unit 107

    OFFICE BUILDING • 1,496 SF
    Value Estimation by Request
    215 Mtn Dr Ste, Destin, FL 32541-2346
    View details
    160th Industrial Park Rd

    160th Industrial Park Rd

    OFFICE BUILDING
    Value Estimation by Request
    160th Industrial Park Rd, Destin, FL 32541-2707
    View details
    215 Mtn Dr Ste, Unit 104

    215 Mtn Dr Ste, Unit 104

    OFFICE BUILDING • 1,188 SF
    Value Estimation by Request
    215 Mtn Dr Ste, Destin, FL 32541-2346
    View details
    215 Mtn Dr Ste, Unit 108

    215 Mtn Dr Ste, Unit 108

    OFFICE BUILDING • 1,130 SF
    Value Estimation by Request
    215 Mtn Dr Ste, Destin, FL 32541-2346
    View details
    151 Regions Way

    151 Regions Way

    OFFICE BUILDING • 2,596 SF
    Value Estimation
    $1,105,000
    151 Regions Way, Destin, FL 32541-5106
    View details
    151 Regions Way

    151 Regions Way

    OFFICE BUILDING • 3,830 SF
    Value Estimation
    $1,085,000
    151 Regions Way, Destin, FL 32541-5106
    View details
    151 Regions Way

    151 Regions Way

    OFFICE BUILDING • 3,328 SF
    Value Estimation
    $1,055,000
    151 Regions Way, Destin, FL 32541-5106
    View details
    215 Mtn Dr Ste, Unit 105

    215 Mtn Dr Ste, Unit 105

    OFFICE BUILDING • 1,192 SF
    Value Estimation by Request
    215 Mtn Dr Ste, Destin, FL 32541-2346
    View details

    Destin, FL Office Buildings Investment Opportunities Market Analysis

    Explore 63 office buildings for sale in Destin, FL, showcased through 9 active listings on our real estate platform. These investment opportunities span a total of 3,801,171,850 square feet of properties for sale, with an estimated market value of $17,242,500.

    Prices for office properties in Destin, FL start at $145,000, averaging $718,437, and reaching up to $3,200,000 — offering options for a variety of budgets and business needs. Daily updated analytics ensure you have the most current data.

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    Browse Office buildings for Sale Near Destin, FL

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    Most Searched ZIP Codes in Destin, FL

    • 32541
    • 32550

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