diff --git a/src/mono/wasi/build/WasiApp.CoreCLR.targets b/src/mono/wasi/build/WasiApp.CoreCLR.targets
index 0c61a7cea23567..7fe3ef641aac2d 100644
--- a/src/mono/wasi/build/WasiApp.CoreCLR.targets
+++ b/src/mono/wasi/build/WasiApp.CoreCLR.targets
@@ -209,6 +209,12 @@
           SourceFiles="$(MicrosoftNetCoreAppRuntimePackRidNativeDir)icudt.dat"
           DestinationFolder="$(WasmAppDir)managed"
           SkipUnchangedFiles="true" />
+    <!-- The wasihost corehost reads the app's runtimeconfig properties from runtimeconfig.bin
+         next to the entry assembly and passes them to the runtime. -->
+    <Copy Condition="'$(_ParsedRuntimeConfigFilePath)' != '' and Exists('$(_ParsedRuntimeConfigFilePath)')"
+          SourceFiles="$(_ParsedRuntimeConfigFilePath)"
+          DestinationFolder="$(WasmAppDir)managed"
+          SkipUnchangedFiles="true" />
   </Target>
 
   <!-- ============================ Per-app wasihost link ============================ -->
diff --git a/src/native/corehost/wasihost/wasihost.cpp b/src/native/corehost/wasihost/wasihost.cpp
index b1b4068b26a43d..baad2e070c90e8 100644
--- a/src/native/corehost/wasihost/wasihost.cpp
+++ b/src/native/corehost/wasihost/wasihost.cpp
@@ -6,6 +6,7 @@
 // real wasi:cli/run main() instead of a JS driver.
 // See https://github.com/dotnet/runtime/issues/130129.
 
+#include <algorithm>
 #include <cstdint>
 #include <cstdio>
 #include <cstring>
@@ -158,6 +159,110 @@ static string_t build_tpa(const string_t& core_root, const string_t& core_librar
     return tpa_list.str();
 }
 
+// ECMA-335 compressed unsigned integer (II.23.2), as written by BlobBuilder.WriteCompressedInteger.
+static bool read_compressed_uint(const uint8_t*& cur, const uint8_t* end, uint32_t& value)
+{
+    if (cur >= end)
+        return false;
+
+    uint8_t b = cur[0];
+    if ((b & 0x80) == 0)
+    {
+        value = b;
+        cur += 1;
+        return true;
+    }
+
+    if ((b & 0xC0) == 0x80)
+    {
+        if (end - cur < 2)
+            return false;
+
+        value = (static_cast<uint32_t>(b & 0x3F) << 8) | cur[1];
+        cur += 2;
+        return true;
+    }
+
+    if ((b & 0xE0) == 0xC0)
+    {
+        if (end - cur < 4)
+            return false;
+
+        value = (static_cast<uint32_t>(b & 0x1F) << 24) | (static_cast<uint32_t>(cur[1]) << 16) | (static_cast<uint32_t>(cur[2]) << 8) | cur[3];
+        cur += 4;
+        return true;
+    }
+
+    return false;
+}
+
+// Length-prefixed UTF-8 string, as written by BlobBuilder.WriteSerializedString.
+static bool read_serialized_string(const uint8_t*& cur, const uint8_t* end, std::string& value)
+{
+    uint32_t len;
+    if (!read_compressed_uint(cur, end, len) || static_cast<size_t>(end - cur) < len)
+        return false;
+
+    value.assign(reinterpret_cast<const char*>(cur), len);
+    cur += len;
+    return true;
+}
+
+// Appends the app's runtimeconfig configProperties (feature switches, RuntimeHostConfigurationOption
+// items, ...) to the init properties. Reads the runtimeconfig.bin that RuntimeConfigParserTask writes
+// (the same file Mono's WASI driver consumes): a compressed count followed by that many key/value
+// serialized strings. Properties already set by the host take precedence. A missing file is not an
+// error.
+static bool add_runtimeconfig_properties(const string_t& path)
+{
+    FILE* file = std::fopen(path.c_str(), "rb");
+    if (file == nullptr)
+        return true;
+
+    std::vector<uint8_t> data;
+    uint8_t buffer[4096];
+    size_t read;
+    while ((read = std::fread(buffer, 1, sizeof(buffer), file)) > 0)
+        data.insert(data.end(), buffer, buffer + read);
+
+    bool read_error = std::ferror(file) != 0;
+    std::fclose(file);
+
+    const uint8_t* cur = data.data();
+    const uint8_t* end = cur + data.size();
+    uint32_t count = 0;
+    bool valid = !read_error && read_compressed_uint(cur, end, count);
+    std::vector<std::string> keys;
+    std::vector<std::string> values;
+    for (uint32_t i = 0; valid && i < count; ++i)
+    {
+        std::string key;
+        std::string value;
+        valid = read_serialized_string(cur, end, key) && read_serialized_string(cur, end, value);
+        keys.push_back(std::move(key));
+        values.push_back(std::move(value));
+    }
+
+    if (!valid)
+    {
+        std::fprintf(stderr, "Failed to read runtime configuration from '%s'\n", path.c_str());
+        return false;
+    }
+
+    size_t host_property_count = s_property_keys.size();
+    for (size_t i = 0; i < keys.size(); ++i)
+    {
+        auto host_keys_end = s_property_keys.begin() + host_property_count;
+        if (std::find(s_property_keys.begin(), host_keys_end, keys[i]) != host_keys_end)
+            continue;
+
+        s_property_keys.push_back(std::move(keys[i]));
+        s_property_values.push_back(std::move(values[i]));
+    }
+
+    return true;
+}
+
 static size_t HOST_CONTRACT_CALLTYPE get_runtime_property(
     const char* key,
     /*out*/ char* value_buffer,
@@ -248,6 +353,12 @@ int main(int argc, char* argv[])
         s_property_values.push_back(ss.str());
     }
 
+    // The app bundle places runtimeconfig.bin next to the entry assembly.
+    string_t runtimeconfig_path = app_path;
+    runtimeconfig_path.append(W("runtimeconfig.bin"));
+    if (!add_runtimeconfig_properties(runtimeconfig_path))
+        return -1;
+
     std::vector<const char*> property_keys;
     std::vector<const char*> property_values;
     for (const std::string& key : s_property_keys)