diff --git a/cranelift/fuzzgen/src/lib.rs b/cranelift/fuzzgen/src/lib.rs
index 26cca8363d..e8e6493146 100644
--- a/cranelift/fuzzgen/src/lib.rs
+++ b/cranelift/fuzzgen/src/lib.rs
@@ -6,7 +6,9 @@ use arbitrary::{Arbitrary, Unstructured};
 use cranelift::codegen::data_value::DataValue;
 use cranelift::codegen::ir::{types::*, UserExternalName, UserFuncName};
 use cranelift::codegen::ir::{Function, LibCall};
+use cranelift::codegen::isa::{self, Builder};
 use cranelift::codegen::Context;
+use cranelift::prelude::settings::SettingKind;
 use cranelift::prelude::*;
 use cranelift_arbitrary::CraneliftArbitrary;
 use cranelift_native::builder_with_options;
@@ -22,6 +24,15 @@ pub use print::PrintableTestCase;
 
 pub type TestCaseInput = Vec<DataValue>;
 
+pub enum IsaFlagGen {
+    /// When generating ISA flags, ensure that they are all supported by
+    /// the current host.
+    Host,
+    /// All flags available in cranelift are allowed to be generated.
+    /// We also allow generating all possible values for each enum flag.
+    All,
+}
+
 pub struct FuzzGen<'r, 'data>
 where
     'data: 'r,
@@ -228,4 +239,56 @@ where
 
         Ok(Flags::new(builder))
     }
+
+    /// Generate a random set of ISA flags and apply them to a Builder.
+    ///
+    /// Based on `mode` we can either allow all flags, or just the subset that is
+    /// supported by the current host.
+    ///
+    /// In all cases only a subset of the allowed flags is applied to the builder.
+    pub fn set_isa_flags(&mut self, builder: &mut Builder, mode: IsaFlagGen) -> Result<()> {
+        // `max_isa` is the maximal set of flags that we can use.
+        let max_builder = match mode {
+            IsaFlagGen::All => {
+                let mut max_builder = isa::lookup(builder.triple().clone())?;
+
+                for flag in max_builder.iter() {
+                    match flag.kind {
+                        SettingKind::Bool => {
+                            max_builder.enable(flag.name)?;
+                        }
+                        SettingKind::Enum => {
+                            // Since these are enums there isn't a "max" value per se, pick one at random.
+                            let value = self.u.choose(flag.values.unwrap())?;
+                            max_builder.set(flag.name, value)?;
+                        }
+                        SettingKind::Preset => {
+                            // Presets are just special flags that combine other flags, we don't
+                            // want to enable them directly, just the underlying flags.
+                        }
+                        _ => todo!(),
+                    };
+                }
+                max_builder
+            }
+            // Use `cranelift-native` to do feature detection for us.
+            IsaFlagGen::Host => builder_with_options(true)
+                .expect("Unable to build a TargetIsa for the current host"),
+        };
+        // Cranelift has a somwhat weird API for this, but we need to build the final `TargetIsa` to be able
+        // to extract the values for the ISA flags. We need that to use the `string_value()` that formats
+        // the values so that we can pass it into the builder again.
+        let max_isa = max_builder.finish(Flags::new(settings::builder()))?;
+
+        // We give each of the flags a chance of being copied over. Otherwise we keep the default.
+        for value in max_isa.isa_flags().iter() {
+            let should_copy = bool::arbitrary(self.u)?;
+            if !should_copy {
+                continue;
+            }
+            builder.set(value.name, &value.value_string())?;
+        }
+
+        Ok(())
+    }
 }
diff --git a/cranelift/fuzzgen/src/print.rs b/cranelift/fuzzgen/src/print.rs
index e74f0f3a84..238f92fcff 100644
--- a/cranelift/fuzzgen/src/print.rs
+++ b/cranelift/fuzzgen/src/print.rs
@@ -1,6 +1,6 @@
 use cranelift::codegen::data_value::DataValue;
 use cranelift::codegen::ir::Function;
-use cranelift::prelude::settings;
+use cranelift::prelude::settings::{self, SettingKind};
 use cranelift::prelude::*;
 use std::fmt;
 
@@ -70,7 +70,9 @@ impl<'a> fmt::Debug for PrintableTestCase<'a> {
 
         write_non_default_flags(f, self.isa.flags())?;
 
-        writeln!(f, "target {}\n", self.isa.triple().architecture)?;
+        write!(f, "target {} ", self.isa.triple().architecture)?;
+        write_non_default_isa_flags(f, &self.isa)?;
+        write!(f, "\n\n")?;
 
         // Print the functions backwards, so that the main function is printed last
         // and near the test inputs for run test cases.
@@ -128,3 +130,33 @@ fn write_non_default_flags(f: &mut fmt::Formatter<'_>, flags: &settings::Flags)
 
     Ok(())
 }
+
+/// Print non default ISA flags in a single line, as used in `target` declarations.
+fn write_non_default_isa_flags(
+    f: &mut fmt::Formatter<'_>,
+    isa: &isa::OwnedTargetIsa,
+) -> fmt::Result {
+    let default_isa = isa::lookup(isa.triple().clone())
+        .unwrap()
+        .finish(isa.flags().clone())
+        .unwrap();
+
+    for (default, flag) in default_isa.isa_flags().iter().zip(isa.isa_flags()) {
+        assert_eq!(default.name, flag.name);
+
+        // Skip default flags, putting them all out there is too verbose.
+        if default.value_string() == flag.value_string() {
+            continue;
+        }
+
+        // On boolean flags we can use the shorthand syntax instead of just specifying the flag name.
+        // This is slightly neater than the full syntax.
+        if flag.kind() == SettingKind::Bool && flag.value_string() == "true" {
+            write!(f, "{} ", flag.name)?;
+        } else {
+            write!(f, "{}={} ", flag.name, flag.value_string())?;
+        }
+    }
+
+    Ok(())
+}
diff --git a/fuzz/fuzz_targets/cranelift-fuzzgen.rs b/fuzz/fuzz_targets/cranelift-fuzzgen.rs
index b20755509d..addf4f71f4 100644
--- a/fuzz/fuzz_targets/cranelift-fuzzgen.rs
+++ b/fuzz/fuzz_targets/cranelift-fuzzgen.rs
@@ -179,9 +179,10 @@ impl TestCase {
 
         // TestCase is meant to be consumed by a runner, so we make the assumption here that we're
         // generating a TargetIsa for the host.
-        let builder =
+        let mut builder =
             builder_with_options(true).expect("Unable to build a TargetIsa for the current host");
         let flags = gen.generate_flags(builder.triple().architecture)?;
+        gen.set_isa_flags(&mut builder, IsaFlagGen::Host)?;
         let isa = builder.finish(flags)?;
 
         // When generating functions, we allow each function to call any function that has
diff --git a/fuzz/fuzz_targets/cranelift-icache.rs b/fuzz/fuzz_targets/cranelift-icache.rs
index 886d158ac1..aa4dc7c793 100644
--- a/fuzz/fuzz_targets/cranelift-icache.rs
+++ b/fuzz/fuzz_targets/cranelift-icache.rs
@@ -48,13 +48,15 @@ impl FunctionWithIsa {
         // a supported one, so that the same fuzz input works across different build
         // configurations.
         let target = u.choose(isa::ALL_ARCHITECTURES)?;
-        let builder = isa::lookup_by_name(target).map_err(|_| arbitrary::Error::IncorrectFormat)?;
+        let mut builder =
+            isa::lookup_by_name(target).map_err(|_| arbitrary::Error::IncorrectFormat)?;
         let architecture = builder.triple().architecture;
 
         let mut gen = FuzzGen::new(u);
         let flags = gen
             .generate_flags(architecture)
             .map_err(|_| arbitrary::Error::IncorrectFormat)?;
+        gen.set_isa_flags(&mut builder, IsaFlagGen::All)?;
         let isa = builder
             .finish(flags)
             .map_err(|_| arbitrary::Error::IncorrectFormat)?;