diff --git a/src/libraries/System.Net.Http/src/System.Net.Http.csproj b/src/libraries/System.Net.Http/src/System.Net.Http.csproj
index c2a4d472ccaa09..ec879372f6fb78 100644
--- a/src/libraries/System.Net.Http/src/System.Net.Http.csproj
+++ b/src/libraries/System.Net.Http/src/System.Net.Http.csproj
@@ -1,7 +1,7 @@
 <Project Sdk="Microsoft.NET.Sdk">
 
   <PropertyGroup>
-    <TargetFrameworks>$(NetCoreAppCurrent)-windows;$(NetCoreAppCurrent)-linux;$(NetCoreAppCurrent)-osx;$(NetCoreAppCurrent)-freebsd;$(NetCoreAppCurrent)-maccatalyst;$(NetCoreAppCurrent)-ios;$(NetCoreAppCurrent)-tvos;$(NetCoreAppCurrent)-browser;$(NetCoreAppCurrent)-wasi;$(NetCoreAppCurrent)-illumos;$(NetCoreAppCurrent)-solaris;$(NetCoreAppCurrent)-haiku;$(NetCoreAppCurrent)-android;$(NetCoreAppCurrent)</TargetFrameworks>
+    <TargetFrameworks>$(NetCoreAppCurrent)-windows;$(NetCoreAppCurrent)-linux;$(NetCoreAppCurrent)-osx;$(NetCoreAppCurrent)-freebsd;$(NetCoreAppCurrent)-openbsd;$(NetCoreAppCurrent)-maccatalyst;$(NetCoreAppCurrent)-ios;$(NetCoreAppCurrent)-tvos;$(NetCoreAppCurrent)-browser;$(NetCoreAppCurrent)-wasi;$(NetCoreAppCurrent)-illumos;$(NetCoreAppCurrent)-solaris;$(NetCoreAppCurrent)-haiku;$(NetCoreAppCurrent)-android;$(NetCoreAppCurrent)</TargetFrameworks>
     <AllowUnsafeBlocks>true</AllowUnsafeBlocks>
     <DefineConstants>$(DefineConstants);HTTP_DLL</DefineConstants>
     <UseCompilerGeneratedDocXmlFile>false</UseCompilerGeneratedDocXmlFile>
diff --git a/src/native/libs/System.Security.Cryptography.Native/opensslshim.c b/src/native/libs/System.Security.Cryptography.Native/opensslshim.c
index 98477b07f0f2fd..92931fb813b30e 100644
--- a/src/native/libs/System.Security.Cryptography.Native/opensslshim.c
+++ b/src/native/libs/System.Security.Cryptography.Native/opensslshim.c
@@ -8,6 +8,12 @@
 #include <stdio.h>
 #include <string.h>
 
+#if defined(__OpenBSD__)
+#include <dirent.h>
+#include <limits.h>
+#include <stdlib.h>
+#endif
+
 #include "opensslshim.h"
 #include "pal_atomic.h"
 
@@ -54,6 +60,80 @@ static void DlOpen(const char* libraryName)
     }
 }
 
+#if defined(__OpenBSD__)
+// OpenBSD's base system ships LibreSSL, which does not implement the full
+// OpenSSL 3.x surface the shim requires. The OpenSSL ports install in parallel
+// under /usr/local/lib/eopenssl<NN>/, where <NN> is the OpenSSL version (e.g.
+// eopenssl35 for OpenSSL 3.5). Each directory ships libssl with its own SONAME
+// (for example libssl.so.37.0), bumped independently of the version number, so
+// the SONAME is discovered within the requested directory rather than hardcoded.
+// The library is opened by absolute path so the matching libcrypto resolves via
+// the library's RUNPATH.
+static void DlOpenEOpenSsl(const char* eopensslVersion)
+{
+    static const char libDir[] = "/usr/local/lib";
+    static const char dirPrefix[] = "eopenssl";
+    static const char sslPrefix[] = "libssl.so.";
+
+    char dirPath[PATH_MAX];
+    int written = snprintf(dirPath, sizeof(dirPath), "%s/%s%s", libDir, dirPrefix, eopensslVersion);
+    if (written < 0 || (size_t)written >= sizeof(dirPath))
+    {
+        return;
+    }
+
+    DIR* dir = opendir(dirPath);
+    if (dir == NULL)
+    {
+        return;
+    }
+
+    // Pick the highest libssl.so.<major>.<minor> in case more than one is present.
+    char libName[NAME_MAX + 1] = { 0 };
+    long bestMajor = -1;
+    long bestMinor = -1;
+    struct dirent* entry;
+    while ((entry = readdir(dir)) != NULL)
+    {
+        if (strncmp(entry->d_name, sslPrefix, sizeof(sslPrefix) - 1) != 0)
+        {
+            continue;
+        }
+
+        const char* version = entry->d_name + sizeof(sslPrefix) - 1;
+        char* end;
+        long major = strtol(version, &end, 10);
+        if (end == version)
+        {
+            continue;
+        }
+
+        long minor = (*end == '.') ? strtol(end + 1, &end, 10) : 0;
+        if (major > bestMajor || (major == bestMajor && minor > bestMinor))
+        {
+            bestMajor = major;
+            bestMinor = minor;
+            strncpy(libName, entry->d_name, sizeof(libName) - 1);
+        }
+    }
+    closedir(dir);
+
+    if (libName[0] == '\0')
+    {
+        return;
+    }
+
+    char libPath[PATH_MAX];
+    written = snprintf(libPath, sizeof(libPath), "%s/%s", dirPath, libName);
+    if (written < 0 || (size_t)written >= sizeof(libPath))
+    {
+        return;
+    }
+
+    DlOpen(libPath);
+}
+#endif
+
 static void OpenLibraryOnce(void)
 {
     // If there is an override of the version specified using the DOTNET_OPENSSL_VERSION_OVERRIDE
@@ -64,9 +144,14 @@ static void OpenLibraryOnce(void)
 
     if ((versionOverride != NULL) && strnlen(versionOverride, MaxVersionStringLength + 1) <= MaxVersionStringLength)
     {
+#if defined(__OpenBSD__)
+        // On OpenBSD the override selects the eopenssl<NN> ports directory.
+        DlOpenEOpenSsl(versionOverride);
+#else
         char soName[sizeof(SONAME_BASE) + MaxVersionStringLength] = SONAME_BASE;
         strcat(soName, versionOverride);
         DlOpen(soName);
+#endif
     }
 
 #ifdef TARGET_ANDROID
@@ -111,6 +196,26 @@ static void OpenLibraryOnce(void)
     {
         DlOpen(MAKELIB("111"));
     }
+#elif defined(__OpenBSD__)
+    // OpenBSD base is LibreSSL; load the OpenSSL ports build from /usr/local/lib/eopenssl<NN>.
+    // Probe the known package directories explicitly, preferring 3.x and trying 4.0 last.
+    if (libssl == NULL)
+    {
+        // OpenSSL 3.6 from ports
+        DlOpenEOpenSsl("36");
+    }
+
+    if (libssl == NULL)
+    {
+        // OpenSSL 3.5 from ports
+        DlOpenEOpenSsl("35");
+    }
+
+    if (libssl == NULL)
+    {
+        // OpenSSL 4.0 from ports (probed but not preferred)
+        DlOpenEOpenSsl("40");
+    }
 #endif
 
     if (libssl == NULL)