diff --git a/.chronus/changes/fix-openapi3-encode-nullable-property-2026-09-18.md b/.chronus/changes/fix-openapi3-encode-nullable-property-2026-09-18.md
new file mode 100644
index 00000000000..6616496eb87
--- /dev/null
+++ b/.chronus/changes/fix-openapi3-encode-nullable-property-2026-09-18.md
@@ -0,0 +1,7 @@
+---
+changeKind: fix
+packages:
+  - "@typespec/openapi3"
+---
+
+Fix `@encode` on nullable properties and parameters in OpenAPI 3.1 and 3.2. The encoding is now applied to the `T` member of `anyOf: [T, { type: "null" }]` instead of being written next to `anyOf`. When the encoding changed the emitted type, like `unixTimestamp`, `seconds` or `@encode(string)` on a number, the old schema rejected every value. When the encoded type stayed a string, like `rfc7231` on `utcDateTime` or `base64url` on `bytes`, it only rejected `null`. `bytes | null` now also gets `contentEncoding` instead of `format`.
diff --git a/packages/openapi3/src/openapi-helpers-3-1.ts b/packages/openapi3/src/openapi-helpers-3-1.ts
index 5df24c7f7d5..6fdee3d5e84 100644
--- a/packages/openapi3/src/openapi-helpers-3-1.ts
+++ b/packages/openapi3/src/openapi-helpers-3-1.ts
@@ -1,13 +1,15 @@
-import type { ModelProperty, Scalar } from "@typespec/compiler";
+import { ObjectBuilder } from "@typespec/asset-emitter";
+import type { ModelProperty, Scalar, Type } from "@typespec/compiler";
+import { getEncode, isNullType } from "@typespec/compiler";
 import { applyEncoding as baseApplyEncoding } from "./encoding.js";
 import type { OpenApiSpecSpecificProps } from "./openapi-spec-mappings.js";
-import type { OpenAPISchema3_1 } from "./types.js";
+import type { OpenAPISchema3_1, Refable } from "./types.js";
 import { isScalarExtendsBytes } from "./util.js";
 
 function getEncodingFieldName(typespecType: Scalar | ModelProperty) {
   // In Open API 3.1, `contentEncoding` is used for encoded binary data instead of `format`.
   const typeIsBytes = isScalarExtendsBytes(
-    typespecType.kind === "ModelProperty" ? typespecType.type : typespecType,
+    typespecType.kind === "ModelProperty" ? getNonNullType(typespecType.type) : typespecType,
   );
   if (typeIsBytes) {
     return "contentEncoding";
@@ -15,12 +17,43 @@ function getEncodingFieldName(typespecType: Scalar | ModelProperty) {
   return "format";
 }
 
+/** Returns `T` for a nullable union `T | null`, otherwise the type itself. */
+function getNonNullType(type: Type): Type {
+  if (type.kind !== "Union") {
+    return type;
+  }
+  const variants = [...type.variants.values()].filter((x) => !isNullType(x.type));
+  return variants.length === 1 ? variants[0].type : type;
+}
+
+function isNullSchema(schema: Refable<OpenAPISchema3_1>): boolean {
+  return "type" in schema && schema.type === "null";
+}
+
 export const applyEncoding: OpenApiSpecSpecificProps["applyEncoding"] = (
   program,
   typespecType,
   target,
   options,
 ) => {
+  // A nullable `T | null` is emitted as `anyOf: [T, { type: "null" }]` in Open API 3.1.
+  // The encoding describes `T` so it is applied to that member and not to the `anyOf` wrapper.
+  const anyOf = (target as OpenAPISchema3_1).anyOf;
+  if (anyOf?.length === 2 && anyOf.some(isNullSchema) && getEncode(program, typespecType)) {
+    const result = new ObjectBuilder(target);
+    result.anyOf = anyOf.map((member) =>
+      isNullSchema(member)
+        ? member
+        : baseApplyEncoding(
+            program,
+            typespecType,
+            member as OpenAPISchema3_1,
+            getEncodingFieldName,
+            options,
+          ),
+    );
+    return result;
+  }
   return baseApplyEncoding(program, typespecType, target, getEncodingFieldName, options);
 };
 
diff --git a/packages/openapi3/test/nullable-properties.test.ts b/packages/openapi3/test/nullable-properties.test.ts
index 51498235192..6b2167d5326 100644
--- a/packages/openapi3/test/nullable-properties.test.ts
+++ b/packages/openapi3/test/nullable-properties.test.ts
@@ -139,3 +139,39 @@ worksFor(["3.1.0"], ({ oapiForModel, openApiFor }) => {
     });
   });
 });
+
+worksFor(["3.1.0", "3.2.0"], ({ oapiForModel, openApiFor }) => {
+  describe("with @encode", () => {
+    it.each([
+      [
+        "DateTimeKnownEncoding.unixTimestamp, int32",
+        "utcDateTime",
+        { type: "integer", format: "unixtime" },
+      ],
+      ["DateTimeKnownEncoding.rfc7231", "utcDateTime", { type: "string", format: "http-date" }],
+      ["DurationKnownEncoding.seconds, int32", "duration", { type: "integer", format: "int32" }],
+      ["string", "int64", { type: "string", format: "int64" }],
+      ["BytesKnownEncoding.base64url", "bytes", { type: "string", contentEncoding: "base64url" }],
+    ])(
+      "@encode(%s) applies to the non-null member of %s | null",
+      async (encode, type, expected) => {
+        const res = await oapiForModel(
+          "Test",
+          `model Test { @encode(${encode}) prop: ${type} | null }`,
+        );
+        deepStrictEqual(res.schemas.Test.properties.prop, {
+          anyOf: [expected, { type: "null" }],
+        });
+      },
+    );
+
+    it("applies to the non-null member of a nullable query parameter", async () => {
+      const res = await openApiFor(
+        `op test(@query @encode(DateTimeKnownEncoding.unixTimestamp, int32) since: utcDateTime | null): void;`,
+      );
+      deepStrictEqual(res.paths["/"].get.parameters[0].schema, {
+        anyOf: [{ type: "integer", format: "unixtime" }, { type: "null" }],
+      });
+    });
+  });
+});